Applied Primatology: Species-Specific Behavior of Captive Japanese Macaques (Macaca Fuscata) Under Varying Zoo Conditions and in the Wild

Iowa State University Capstones, Theses and Retrospective Theses and Dissertations Dissertations

1-1-2004

Applied primatology: species-specific behavior of captive Japanese macaques (Macaca fuscata) under varying zoo conditions and in the wild

Kristina Ralene Walkup Iowa State University

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Recommended Citation Walkup, Kristina Ralene, "Applied primatology: species-specific behavior of captive Japanese macaques (Macaca fuscata) under varying zoo conditions and in the wild" (2004). Retrospective Theses and Dissertations. 20301. https://lib.dr.iastate.edu/rtd/20301

This Thesis is brought to you for free and open access by the Iowa State University Capstones, Theses and Dissertations at Iowa State University Digital Repository. It has been accepted for inclusion in Retrospective Theses and Dissertations by an authorized administrator of Iowa State University Digital Repository. For more information, please contact [email protected]. Applied primatology: Species-specific behavior of captive Japanese macaques (Macaca fuscata) under varying zoo conditions and in the wild

Kristina Ralene Walkup

A thesis submitted to the graduate faculty

in partial fulfillment of the requirements for the degree of

MASTER OF ARTS

Major: Anthropology

Program of Study Committee: Jill Pruetz, Major Professor Matthew Hill Bonnie Bowen

Iowa State University

Ames, Iowa

2004

Graduate College Iowa State University

This is to certify that the master's thesis of

Kristina Ralene Walkup has met the thesis requirements of Iowa State University

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TABLE OF CONTENTS

ABSTRACT w CHAPTER 1. INTRODUCTION 1 Research Questions Significance of Study

CHAPTER 2. LITERATL:TRE REVIEW 9 Species-Specific Behavior Requirements for Primates in Captivity Implications and Importance of Maintaining Healthy Captive Populations Japanese Macaques Summary

CHAPTER 3. METHODOLOGY 29 Subjects and Study Sites Data Collection Methods Analysis

CHAPTER 4. RESULTS AND DISCUSSION: NON-SOCIAL BEHAVIORS 38 InactlVlty Move Feeding Object Manipulation Autogroom

CHAPTER 5. RESULTS AND DISCUSSION: SOCIAL BEHAVIORS SS Allogroom Play SeXual ACtlVlty Agonism

CHAPTER 6. S RY AND CONCLUSIONS 77 Summary Recommendations Significance of Study

APPENDIX: ETHOGRAM 92

REFERENCES 93 1V

ACKI~TOWLEDGEMENTS 101 v

ABSTRACT

Two groups of captive Japanese macaques (Macaca fuscata) were studied to determine whether these captive populations display species-specific behaviors. This was determined by comparing captive behavior at the Blank Park Zoo (Des Moines, IA) and

Minnesota Zoo (Apple Valley, l~~I~T), to the literature on wild Japanese macaques. Data collected include an activity budget, reporting time spent performing typical primate behaviors, and whether the monkeys show aberrant behaviors typically seen in captive situations. Both factors were analyzed to determine the welfare of the populations and their similarity to wild conspecifics. The two troops differ in enclosure type and size, male: female ratio, and zoo management methods. It was hypothesized that captive macaques will be similar to wild macaques regarding behaviors expressed, but the frequency of behaviors will differ from wild conspecifics. This hypothesis was not rejected, with all wild behaviors present, but to varying degrees within each population. In particular, monkeys at both zoos exhibited high amounts of inactivity, which is possibly linked to the lack of infants and foraging opportunities. Foraging at the Blank Park Zoo was found to be significantly different from wild monkeys, though at the Minnesota Zoo, monkeys foraged to a similar degree as in the wild. Grooming, both alogrooming and autogrooming, was observed to differ for the captive monkeys in comparison to wild monkeys, in that wild monkeys spend much more time engaged in social grooming and a very small amount of time autogrooming.

It is hypothesized that the lack of competition in the zoo setting has reduced the need to develop extended alliances through social grooming. The addition of infants, and further environmental enrichment may help reduce several of these differences between wild and captive monkeys. 1

CI~[APTER 1. INTRODUCTION

Japanese macaques (Macaca fuscata) are one of the best studied species of nonhuman primate (Fedigan and Asquith 1991). Specific behavioral patterns characteristic of these monkeys are well documented, thus our knowledge of how these monkeys behave under natural conditions is extensive. However, when animals are taken out of their natural context and placed in captive situations, behavioral patterns are likely to change. The captive environment differs from the wild environment in a number of ways. Animals no longer have to search for food, defend themselves from predators, or search for shelter and protection. Additionally, zoo environments often do not allow the animals space that is similar to the wild, resulting in crowded conditions. The one constant between the two environments, in cases where species are socially housed in captivity, is the opportunity to interact with conspecifics. However, social interactions may also be skewed by captivity.

Zoo environments, though seemingly protective, may also be threatening in that there is no escape for individuals from a dominant conspecific. Zoo animals are regularly under the gaze of zoo patrons —who often may add tension to the situation. Perhaps even more pervasive is the issue of boredom. Zoos do not often provide animals the same level of stimuli as that in the wild, including challenges, choices, or opportunities for change.

Captive animals can easily predict when and what they will be fed; their social group will not be varied; and natural functions such as breeding are often prohibited. Clearly, due to these factors, there is reason to expect behavioral differences between captive and wild populations. In zoos, the behavioral change is typically negative for individuals, resulting in animals with high rates of inactivity anal abnormal behaviors (Swaisgood et al. 2003). This study is aimed at examining the species-specific behavior of captive Japanese macaques in 2 zoos to understand the behavioral flexibility of the species and to determine what factors in the artificial environment are affecting the monkey's experiences.

Research Questions

This study allows several research questions to be addressed. In general, the main goal of the study is to determine if captive Japanese monkeys display species-specific behavior as seen in the wild. This goal can be broken down into specific areas. Species- specific behaviors for Japanese macaques are diverse and include grooming, playing, aggression, affiliation and maintenance of the dominance hierarchy within the troop. It is clear to any observer that such behaviors are present in captive populations. The question to be addressed is whether these activities are present in the same proportion in captivity as they are in wild populations. Is the temporal activity budget of wild Japanese macaques comparable to that of their captive conspecifics? It is hypothesized that all species-specific behaviors of wild populations will be present in the captive populations, but to varying extents.

To fully understand the time activity budget of Japanese macaques it is necessary to explore environmental factors influencing their behavior. Enclosure size, privacy from visitors and other monkeys, climbing opportunities, food choices, sex and age ratios, enrichment, and the presence or absence of kin groups are all key factors which could influence the behavior of both individual members and the entire troop. To tease out these effects, two troops of Japanese macaques were studied at different zoos, the Minnesota Zoo

(Apple Valley, Minnesota) and the Blank Park Zoo (Des Moines, Iowa), which differed regarding most of the above factors. 3

In the wild, studies have shown that kin relations .are the most important determinant of social behavior (Pavelka 1993). Will this remain true in the zoo setting? Both zoos

studied were effectively non-breeding facilities at the time of data collection. This has the

possibility of being detrimental to the population since the most important kin relation in

Japanese macaque society is that of mother and daughters. How will the lack of new

offspring affect the relations between individuals in the zoo? will social relations among

individuals be drastically altered from the wild state? will the lack of extended kin groups

destabilize the troop or will the monkeys find a new way to create alliances?

Directly tied to kin groups is the dominance hierarchy. Kin are essential for support

and maintenance of this hierarchy that is characteristic of Japanese macaque society

(watanabe 2001). How is dominance determined and maintained in captivity? Will only

those animals with known kin present be able to ascend in the hierarchy? Since dominance is

an integral part of the species-specific behavior of this species, it will be crucial to investigate

these questions. In the wild, Japanese macaques have a separate male and female dominance

hierarchy (Pavelka 1993 ). At both Minnesota and Blank Park, however, the sex ratio is

skewed, with a larger percentage of females in both situations. Thus interactions between

and among sexes may be altered from wild conditions. As well, the age ratio is abnormal in

comparison. to wild conditions, with no juveniles in either troop. This may also alter the

behavior of the monkeys.

The physical environment of the zoo and enrichment activities planned by the keepers

may also influence macaque behavior. Rocks, trees, logs, and water are present in both

habitats but to different extents. The amount of terrestrial and arboreal space also varies

between the two contexts. How do these factors influence species-specific behaviors? 4

In general, this study aims to document and understand the full repertoire of Japanese

macaque behavior as seen in the captive situation. In order to determine if the behaviors are

similar to those observed in the wild (Maruhashi 1981; Yotsumoto 1976), or in free-ranging,

provisioned situations (Pavelka 1993; Fedigan and Asquith 1991), captive behavior and all

factors that may be of influence were analyzed. It is hoped that by determining whether or

not these populations are displaying species-specific behaviors, the general welfare and

psychological health of the troops can be ascertained.

Significance of Study

This study is significant to three interrelated disciplines: primatology, zoo biology,

and anthropology. Inferences can be made about certain aspects of human behavior by

studying captive primates, which is applicable to physical and cultural anthropology. In particular, the possible similarities of living primates to our human ancestors make them

invaluable study subjects.

primatology concerns itself with every aspect of study regarding the order Primates.

This study is an example of applied primatology, which is the "application of behavioral

knowledge in the primate realm" (Maple and Finlay 1989:482). It seeks to use knowledge of a species to solve management problems and provide the best possible captive environment for the animals. These management problems include how to reduce stereotypical behaviors, increase reproductive success, and, in general, how to promote species-specific behaviors.

This study can contribute significantly to the conservation of this species. Japanese macaques are a threatened species in the wild and are part of the Species Survival Plan coordinated by the American Zoological Association. Wiese and Hutchens (1997) describe the two main components of the Species Survival Plan: population management and 5 husbandry, and conservation. This involves maintaining healthy populations by using animal exchange programs to promote genetic diversity within captive populations. This diversity is essential to maintaining self-sustaining captive populations, which in turn are crucial to animal repatriation projects and conservation efforts. Even regarding those species such as

Japanese macaques for which there is no desire to transplant captive animals to the wild, the

Species Survival Plan is still important in maintaining self-sustaining populations. Fa

(1986:197) also notes that the goal of all captive programs is "to protect the species in its

natural state." Thus captive populations should be displaying species-specific behaviors and

reproducing to maintain aself-sustaining and genetically variable population. Though

reproduction of the macaques at Blank Park is being suppressed, this is not the case for the

monkeys at Minnesota. This population is currently not reproducing, though the zoo hopes it

will.

Zoo biology overlaps with primatology and extends it by adding the zoo visitors to the picture (Hediger 1969). There is no question that people and animals are intrinsically

linked at zoos. Zoo biology deals with the interaction between humans and animals. Zoo patrons have an enormous effect on the temperaments of zoo animals. The noise the people create, their constant gaze and even their physical intrusions into the animals' environment

will have an effect on the animals. For example, patrons may introduce dangers to the animals by feeding them, disrupting their diet and making it impossible to track a particular animal's feeding record. Additionally, this can introduce disease to the animal, especially primates (Croke 1997). Studies have also demonstrated that the proximity of the animals to the public, lack of privacy, and number of visitors negatively affects species-specific

behaviors and reproduction (Swaisgood et al. 2003}. The animals in turn may have an effect 6 on the visiting public, including their behavior at the zoo and their feelings towards the animals and conservation. Croke (1997:93) documented the affect of naturalistic exhibits on the zoo patrons, "over and over, as I visited zoos, I witnessed people speaking reverentially and quietly before exhibits that were truly natural." Scientific study supports this observation. Visitor perception of the animals as undignified and unhappy is directly correlated to the lack of a naturalistic enclosure (Maple and Finlay 1986). Furthermore, zoos are intended to be educational centers for the public. Zoo patrons will not learn accurate information about a species if the animals are not displaying their natural behaviors.

Anthropologically, this study is of value in several meaningful ways.

Anthropologists study other members of the order Primates in an effort to better understand our own evolution and behavior. In particular, there are many features of Japanese macaque society, such as organization, affiliation, aggression, homosexuality, and dominance that are similar to that seen in human societies. Japanese macaques are also one of the few monkey species in which cultural transmission has been well documented (Hirata 2001). For example, wild monkeys in Japan have a culture of washing sweet potatoes in saltwater to remove sand. This behavior developed spontaneously with one individual, eventually spreading to the other community members through learning (Hirata 2001). While, it is possible that cultural traditions are in place in captive populations, it is nearly impossible to address this here due to the lack of offspring in both zoo settings. However, maintenance of a healthy zoo population is key to such behavior arising in the first place.

Behavior can be expressed in both normal and abnormal ways. Perhaps one of the most interesting comparisons that have been made between humans and captive animals regards the presence of abnormal behaviors. Morris (1969) in his appropriately entitled book, 7'he Human Zoo, compares the evils and abnormalities observed in human society to those recorded in zoos. In reference to human atrocities, he states, "the zoo animal in a cage exhibits all those abnormalities that we know so well from our human companions" (Morris

1969:8). He continues to argue that humans do not live in the natural environment in which our species evolved, but rather an artificial "human zoo" (Morris 1969:8). By this comparison, the evils of society can be understood as the result of the suppression of humans' own species-specific behaviors. However, it is not only in human atrocities that we can see the problems of deviating from species-specific behaviors. Humans evolved in a landscape and environment that was very different from the way most people live today. In particular, Bower (2003) discusses how traditional sleeping patterns in which people sleep for onl3~ brief intervals of time, resting several times during the day, may be more beneficial than the eight hour straight sleep cycles that many of us endeavor to, but fail to get. Other species-specific behaviors such as breast-feeding and parents co-sleeping with infants have been shown to provide health benefits including both a reduction in breast cancer and Sudden

Infant Death Syndrome, respectively (Whitaker 2003). In sum, humans, in some regards, cannot be separated from the natural world. We are still more suited to our species-specific behaviors than to artificial replacements.

The study of nonhuman primates under varying conditions provides insight into the amount of behavioral flexibility species exhibit as well as the effect of the environment on behavior. In particular, studies such as this show the importance of both nature and nurture in determining the behavior of individuals (cove and Carpenter 1982). Though species- specific behaviors are "natural" to Japanese macaques, the environment of captivity may nurture different behaviors, thus creating captive conspecifics that are unlike wild 8 counterparts. de Waal (1996) discusses a similar study involving comparisons between captive and wild chimpanzees. His research demonstrates that the behavioral flexibility of the species allowed for significant differences to arise in the captive setting. Captive females in particular, de Waal (1996) found, show a higher degree of affiliation than in the wild.

More important, this behavioral flexibility is crucial to understanding the evolution of our species. Without this ability to adapt to a stable and confined way of life, humans would never have "made the monumental step towards life in permanent settlements" (de Waal

1996:169).

The behavioral plasticity of primates, including Japanese macaques, makes adaptations to circumstances such as captivity possible. In fact, this is one of the characteristics of the order Primates; primates are not overly specialized or resistant to change. Instead, primates can adapt to changing environments. The expansion of many wild

Japanese macaques into suburbs highlights this facet of their behavioral ecology.

Additionally, the macaques at the Texas Snow Monkey Sanctuary have developed their own culture in response to a different environment. These monkeys have alarm calls for rattlesnakes and have developed foraging strategies to deal with prickly pear cactus (Pavelka

1993). Such plasticity also makes generalist species, such as Japanese macaques, able to adapt to the zoo environment. Thus, as long as the zoo provides a stimulating environment for these species, they should be able to adapt reasonably well to captivity. 9

CHAPTER 2. LITERATURE REVIEW

Japanese macaques are extremely well studied (Fedigan and Asquith 1991). They have been studied extensively in the wild in Japan (Altmann 1958; Maruhashi 1981;

Yotsumoto 1976), in afree-ranging situation in Texas (Fedigan and Asquith 1991; Pavelka

1993), and in many captive situations (de Vries and Taylor 1989; Lunardini 1989; Shino et al. 1998). Similarly, many studies have explored the importance of maintaining species- specific behaviors in captive animals (Swaisgood et a12003; Maple and Finlay 1989; Roder and Timmermans 2002; Veasey et al. 1996). This study, though, is unique in exploring the species-specific behaviors of Japanese monkeys through a comparative approach in anthropological perspective.

Species-Specific Behavior

The maintenance of species-specific behavior is crucial for any wild animal held in captivity. Species-specific behaviors are simply defined as behaviors expressed in wild populations, which most members of the population express (Bayne 1989). Erwin and Deni

(1979:2) note the importance of studying species-specific behaviors stating, "ideally, evaluation of effects of captivity on behavior would be accomplished by direct comparison of species-typical behavior in the wild with the form and frequency of the same behaviors in various captive settings." A comparison between the activity budgets of captive animals to wild conspecifics is an effective way to determine how the captive environment is shaping behavior (Melfi and Feistner 2002; Maple and Finlay 1989). However, it is difficult to define the natural behavior of a species. Behavior and time spent in those behaviors can vary significantly throughout the species' range and through seasons (Melfi and Feistner 2002).

Despite these problems of assessing what is the natural behavior for a species, many authors 10 agree that accounting for species-specific behavior is a valuable way to determine the welfare of captive .populations (Hediger 1969; Maple and Finlay 1989; Chang et al. 1999). Since the expression of species-specific behavior is linked to what is natural for the animal, many attempts to promote these behaviors endeavor to make the captive environment as natural as possible. Adding trees, water, rocks, and vegetation contributes to the complexity of the environment, which benefits the animals. Pereira et al. (1989) noted that naturalistic enhancement of a sifaka (P~opithecus verreauxi) enclosure clearly changed activity patterns.

They documented an increase in activity, feeding, play, and body weight. These additions added to the complexity of the captive environment, which was characteristic of the natural environment. Forests and other habitats that primates occupy are full of stimuli that occupy the time of the animals. The main weakness with most captive environments is the lack of suitable stimuli for the animals. In a study conducted on captive orangutans, Tripp (1985) noted that there is a positive correlation between activity level and the complexity of the environment.

Specifically, captive habitats resembling the habitat of wild conspecifics are thought to promote species-specific behaviors and increase the well-being of the group. Chang et al.

(1999) tested this idea by exploring how mandrill behavior changed when a group of captive mandrills (Mandrillus sphinx) were transferred from anon-ecological indoor facility to an environment that more closely resembled their natural environment. Foraging and locomotion patterns increased once they moved to the naturalistic environment, but other behaviors such as playing and social interaction decreased. A significant change was also seen in the amount of abnormal behaviors reported, with 3% of their time spent occupied in abnormal behaviors in the indoor exhibit and no abnormal behavior in the naturalistic 11 environment (Chang et al. 1999). Swaisgood et al. (2003) emphasize that enclosure design needs to be much more complex rather than simply appearing natural if it is to maintain long lasting appropriate behaviors: They explain that when designing enclosures to meet species- specific requirements, space, enclosure complexity (e.g., topography, substrate, vegetation and barriers) and microclimate variation need to be addressed. Of course all of these are features that the animal would find in its natural habitat, but they may not be so obvious to zoo designers. In the wild, natural behaviors evolved to meet constant changing stimuli and challenges. Any captive environment attempting to mimic the natural state of the animals needs to take factors such as food choices, novelty and availability of social interactions into consideration. Maple and Finlay (1989) distinguish between "soft" and "hard" zoo environments. "Hard" environments are barren, artificial and not stimulating for the animals, while "soft" environments are more naturalistic and seemingly comfortable for the animals.

The "soft" enclosure design at the Woodland Park Zoo (Seattle, Washington) is an excellent example. The technique used to create the enclosure for the gorillas at this zoo is referred to as "landscape immersion" which invokes a wilderness feeling for both the visitors and hopefully the animals (Maple and Finlay 1989). The Oregon Zoo (Portland, Oregon) has made their enclosures more naturalistic by allowing the animals some control and choices in their day-to-day environment. Markowitz's (1979) study of gibbon (Hylobates lay) feeding behavior at this zoo revealed that when the animals are given the option of freely available food verses food that they have to work for, the animals routinely choose the latter, more stimulating option. 12

Requirements for Primates in Captivity

The maintenance of species-specific behavior in captivity must be explored by examining the animals' physical and mental needs. These needs are interrelated and the overall health of the animals cannot be maintained unless both requirements are addressed.

Captive animals in zoos are faced with many challenges that wild animals do not encounter.

These challenges include dealing with a limited and restricted amount of space, constant confinement with the same animals, stress induced by being on display, and the lack of stimulating activity. Many of these challenges can be overcome by simple management strategies,. which would increase the physical and psychological well-being of the animals.

Humans have been discounting the effort required to house and care for animals in captivity ever since the practice began. Obviously, all animals require an environment that fits their physical needs, and for some species (maybe all) their psychological needs as well.

The first priority in caring for a primate is the animal's physical care. First, it is necessary to have a habitat that allows the animal mobility. Animals need exercise just as humans do if they are to stay healthy. Most primates spend at least some of their time in arboreal situations, thus captive primates .also need trees or some sort of apparatus to climb. Allowing for vertical climbing space in the cage is a healthy and space-effective way to increase enclosure usability for arboreal to semi-arboreal animals. 'Cages that are too small and lack mental stimuli result in abnormal behaviors such as pacing and rocking~(Novak et al. 1994).

Related to how much space is allotted for the animals is how the enclosure is secured.

The health and safety of both the visitors and the animals depends on enclosures, which keep animals and people in their designated areas. In addition to simply ensuring that people physically cannot enter into the cages of the animals, precautions also must be taken to avoid 13 communicable diseases, garbage, and food from entering the enclosure. Primates are easily susceptible to many human diseases, and captive animals can be harmed by human garbage if they swallow indigestible items (Croke 1997). Thus, it is imperative that protective barriers are In place.

Nutrition and exercise are also key factors to maintaining the physical health of the animals. Though exercise is clearly linked to enclosure size, a large enclosure does not necessarily guarantee that the animal will use the space effectively for exercise. Inactivity is one of the main problems facing animals in zoos; hence, these animals do not receive the same amount of exercise as wild animals, and thus are at risk of obesity and other health problems (Bennett and Davis 1989). Inactivity is usually the result of a lack of foraging opportunities. For instance, captive primates are usually fed commercial primate pellet food.

This pellet food is often distributed at certain times of the day and is readily available. Thus captive primates do not need to expend energy in searching for their food as those animals in the wild would. For many wild primates nearly half of their waking hours are spent in foraging activities (Maple and Finely 1989). Also, many wild primates eat a wide variety of foods, including fruits, leaves, insects, and some meat. The procurement of these foods involves exercise and results in a nutritious and stimulating diet. Though the commercial food does provide for physical dietary needs, it does not increase activity, nor is it stimulating for the animals. Nutrition and exercise of captive animals can be advanced simply through following the species-specific repertoire of the animals. As Pruetz and

McGrew (2001:19) explain, "seeking, processing and ingesting food is a vital component of chimpanzee daily life." Captive primate programs need to consider this .when designing feeding programs. Rather than feeding being perceived as simply a necessity for 14 nourishment, it should be viewed as a valuable enrichment tool, which can help to elevate boredom. Zoos should provide the best captive environment possible, in that it should resemble the natural environment, including a variety of foods and food procurement activities. Many facilities have added foraging devices to the animals' cages. These devices include termite mounds, artificial gum-trees, puzzle boxes, and food dispensers (Reinhardt

1993a).

A problem zoos have though is their focus on simulating the natural environment because of zoo visitors and their focus on aesthetics, rather than what is most important to the animals. This leads some zoos to avoid artificial enrichment devices, such as plastic toys and puzzle feeders. When designing enclosures, zoo managers need to consider what will most stimulate the animals, be it either natural or artificial. Both types of enrichment can be beneficial. Artificial food devices can help to promote species functional behaviors.

Swaisgood et al. (2003) noted that functionalism rather than a complete adherence to naturalism is more important to captive animals. Functionalism simply refers to the animal being able to interact with their environment in a way that is functionally similar to how the animal would act in the wild (Swaisgood et al. 2003). Thus, opportunities for increased foraging time may serve to functionally stimulate the captive animal cognitively and physically in a way similar to their wild counterparts. However, other studies point to natural food enrichment (e.g., whole or varied foods) as being more beneficial to stimulating the individuals (Reinhardt and Roberts 1997). It may be possible that a combination of both artificial and natural enrichment may be the best option in many situations.

The physical needs of primates in captivity are clearly linked to the psychological needs of the animal. But how are these needs determined? Thomas and Lorden (1989) begin 15 their discussion on this subject by examining how we know if animals even have psychological needs. They note, "that awareness of one's existence is a prerequisite to knowing or having psychological well-being" (Thomas and Lorden 1989:12). Thus, in order to consider the psychological needs of an animal, it must first be determined that the animal is conscious of itself and its environment. Thomas and Lorden (1989) conclude their discussion on this topic by noting that there is no conclusive evidence of self-awareness in monkeys, as there is in apes. Most monkey species have not passed the "mirror test;" this is the ability to correctly identify oneself in a mirror and considered a prerequisite of self- awareness. Thomas and Lorden (1989) admit though that just because self-awareness has not been proven does not mean that this capacity is not present. Perhaps as Shumaker (2002) suggests for studies on the cognition of apes, the typical methodology for testing monkey cognition is simply not appropriate to their species.

Even if it has not been demonstrated that monkeys possess a concept of self, it certainly has been well documented that a lack of mental stimulation results in physical deterioration, abnormal behaviors, and reproductive failure (Erwin and Deni 1979). Primates in particular have been shown to have psychological needs that must be satisfied if they are to not appear listless and bored. Some species seem more affected than others. For instance, many zoo visitors have reported seeing a sad or blank look in the eyes of a gorilla, but few people would make the same observation of a fish. Both the physical and psychological well-being of primates cannot be ignored if a facility wishes to have a healthy population.

Robert ~erkes, the first to study chimpanzees (Pan troglodytes) in the United States, realized this fact in 1923. Brent (2001:3) describes Yerkes' concern stating, "chimpanzees need

...spacious outdoor areas with shelter, cleanliness, a variety of foods, species companionship, 16 human companionship and opportunities for work and play." This is true of other primate species as well. The 1985 amendment to the Animal Welfare Act recognized this by stipulating that the physical environment of nonhuman primates must enhance psychological well-being (Bayne 1989). Bayne (1989) discusses ways in which to determine the mental health of an animal. Reproductive success, body weight, general physical appearance, the presence of stress hormones, and behavioral observations are ways in which to monitor the mental state of an animal. Since we certainly cannot ask an animal about its mental state, these methods are crucial to assessing a captive population of primates.

The presence of abnormal behaviors is probably the most self-evident proof of an unhealthy mental state for an animal. Erwin and Deni (1979) discuss two categories of abnormal behavior, qualitative and quantitative abnormalities. Qualitative abnormalities occur only in the captive setting. There is a long list of these abnormalities associated with captive primates, including bizarre postures, self-biting, floating limbs (where one limb will slowly float upward seemingly unnoted by the animal), self-clasping, saluting or eye poking, pacing, head tossing, rocking, coprophagia, and paint eating. Sexual dysfunction, including inappropriate sexual positioning and loss of sexual motivation, also characterizes captive primates (Erwin and Deni 1979). Quantitative abnormalities, also referred to as stereotypical behaviors, are behaviors that are present under natural conditions, but at different rates than those seen in captivity. Extended inactivity, eating disorders (over and under-eating, and excessive drinking), and hyper-aggression are all examples of this type of abnormality

(Erwin and Deni 1979). 17

Implications and Importance of Maintaining Healthy Captive Populations

Maintaining species-specific behavior is essential for both zoo education and for animal reintroduction programs. The maintenance of species-specific behavior is important for zoo education in that patrons often learn about wild animals from what they see in zoos.

Candland and Bush (1995) assert that more people visit zoos each year than attend professional sporting events. With this many people visiting zoos, it is crucial that the information visitors learn about the animals at the zoo is representative of what occurs in nature. If these behaviors are not maintained it is very possible for the zoo to produce misinformation regarding the species, thus hindering education and possibly conservation efforts. For example, those zoo visitors who see primates throw feces probably assume this is a common behavior typical of wild primates. What the zoo visitor would fail to learn in this instance is that wild primates do not normally behave in this manner and this is an aberrant behavior in captive primates (Erwin and Deni 1979). This type of situation does not produce respect and empathy for the animals and may negate attempts to interest zoo patrons in conservation efforts. Similarly, it is important to maintain species-specific behaviors especially if the zoo is a participant in the Species Survival Plan. This project depends on animals remaining healthy and reproductively fit. Some zoos are also interested in reintroducing animals into the wild. Reintroduction programs will not be successful if the animals have lost the ability to survive in the wild by not learning or practicing necessary behaviors (Stoinski et al 1997). Though this option may not be entirely realistic for some species, it may be the one hope left for eventually restocking species if wild populations are destroyed. 18

Japanese Macaques

Japanese macaques are one of the most successful of the nineteen macaque species, occupying a niche that no other non-human primates have managed. This species lives in a high, temperate latitude habitat in Japan (Hill 1974). Their ability to live at this latitude classifies these macaques as generalists —due to their ability to adapt to Japan's four seasons.

Japanese macaques have adapted to the cold winters by growing thick coats and by practicing

behaviors such as sunbathing and soaking in hot springs. They are also generalized in their diet, employing a large range of food items to satisfy their dietary needs, mostly eating leaves

but also nuts, berries, bark, insects, crabs, and eggs (Fedigan 1976). These items can be

found in their natural habitat, which is a mountainous broad-leafed or evergreen forest.

These medium sized (females: 8.3 — 18.0 kilograms, males: 11.0 — 18.0 kilograms)

monkeys are characterized by grayish to brownish red hair and red faces (Rowe 1996). They

are described as being both terrestrial and arboreal quadrupeds (Fedigan 1976). Like all

cercopithecines, they have cheek pouches and noticeable sitting pads or ischial callosities.

Unlike many primate species though, they have a very short tail. Dimorphism between males

and females is apparent, with adult males possessing larger bodies and canines than females.

These macaques are seasonal breeders, with breeding beginning around September and

ceasing around February. Females mate during estrus, which Pavelka (1993:96) describes as

"that period in which females may be motivated and/or willing to mate." She also notes that

there is no pattern as to when the females may come into estrus or how long it will last

(Pavelka 1993). Some females are only in estrus for one day during the breeding season;

others are in estrus during the entire season. Physical signs of estrus include redder faces and

genital regions; the latter may be slightly swollen. This sexual swelling may not be obvious 19 to human observers, but presumably it is perfectly clear to conspecifics (Pavelka 1993).

During estrus, males and females often form a consortship, which is a type of extended contact between the individuals, including more than just sexual activity, but also grooming, close proximity, feeding, and traveling together. Pavelka (1993) notes that there is much variability in the length of the consortship, ranging from hours to weeks. Copulation between Japanese macaques occurs via series mounting, which involves many mounts (5-15) spread over a long period of time and eventually resulting in ejaculation. Between mounts, the pair sits in close proximity (Pavelka 1993). Both males and females take an active role in the consortship, with the consortship often being initiated by either the male or the female

(Pavelka 1993). Consortships also occur between females. An intense and prolonged bond between individuals and mounting behavior also characterizes these consortships. Females in this type of consortship alternate the role of mounter/mountee, with the mounter rubbing her genital region on the mountee (Pavelka 1993).

Currently, there are two subspecies classified as Japanese macaque, M. fuscata fuscata and M. fuscata yakui. T'he former is found throughout Japan, while the latter subspecies is only found on the island of Yakushima, and is also referred to as the Yakuzarus

Japanese macaque. The differences between subspecies are not based on behavior but on slight differences in appearance. Yakuzarus macaques are stockier, and their fur is darker

(Hill 1974). Not all are in agreement on the classification of these subspecies (Nozawa et al.

1991). Nozawa et aL (1991) note that there is very little genetic evidence of a subspecies split. Further molecular studies are underway to determine if there is any genetic reason for the classification of two subspecies (Domingo-Roura et a12004). 20

Since the 1940s, Japanese researchers have been collecting data on Japanese macaques' behavior and ecology. The Japan Monkey Center was formed in 1956 with the specific goal of understanding Japan's native primate species. Part of the excitement that led to the opening of this establishment stemmed from the discovery of the highly organized society of the Japanese macaque. Scientists studying these animals noted the similarity to human societies and concluded:

That by close examination of these primate societies, it would be possible to deduce not only the origin of human society and organization, and the basic organizing rules and principles involved, but also the line of evolution towards human beings (Watanabe 2001:405)

This ambitious goal of Japanese researchers may not have been realized, but one cannot dispute the fact that Japanese macaques have a very organized and complicated social system.

Japanese monkeys today live in three main environments: their natural wild habitat in

Japan (in which most troops are provisioned with food), afree-ranging but restricted habitat in Texas (provisioned) known as the Arashiyama West Colony (or Texas Snow Monkey

Sanctuary), and in zoos and research facilities across the globe. Table 2.1 lists Japanese macaque colonies in zoos in the United States as well as the wild and free-ranging populations referred to in this study.

Wild, unprovisioned Japanese macaques typically live in multi-male, multi-female social groups with an average troop size of 40-50 individuals (Fedigan 1976; Maruhashi

1981). Since provisioning of troops began, it is now common to find troops of more than one hundred individuals (Fedigan 1976; Kurland 1972). These provisioned monkeys are not 21 truly considered wild, since their subsistence is now dependent on humans. Provisioning is in fact what was responsible for the need for the Arashiyama West Colony.

Table 2.1. Troop composition in Japan and the United States Site/Troop Location Description Troop size Yakushima Ko-troops Wild — unprovisioned 47 Island, Japan Suzuka Kaminyu2 Wild —provisioned 81 mountains, Japan Takagoyama Takagoyama3 Wild —provisioned 67 area, Japan

4 Takasakiyama, Takasakiyama Wild —provisioned 350 Japan Arashiyama, Arashiyama EastS Wild —provisioned > 200 Japan Arashiyama W est6 Dilley, TX Free-ranging —provisioned >300 Blank Park Zoo Des Moines, IA Zoo 21 Buffalo Zoological Buffalo, NY Zoo 5 Gardens' Capron Park Zoo' Attleboro, MA Zoo 4 Central Park Zoo' New York, NY Zoo 12 Cincinnati Zoo & Cincinnati, OH Zoo 11 Botanical Garden' Detroit Zoological Detroit, MI Zoo 15 Institute' Mill Mountain Zoo' Roanoke, VA Zoo 3 Milwaukee County Milwaukee, MI Zoo 24 Zoological Gardens' Apple Valley, Minnesota Zoo Zoo 15 MN NEW Zoo' Green Bay, WI Zoo 3 Pittsburgh Zoo & Pittsburgh, PA Zoo 4 Aquarium' 1 Maruhashi (1981) 5 Huffman (1991) 6 2 Kurland (1972) Fedigan (1991) 3 Yotsumoto (1976) International Species Information System (2004) 4 Furuya (1957)

Provisioning at the Arashiyama site near Kyoto eventually led to an increase in group size in the 1960s and 1970s, with the large group eventually fissioning into two groups (A and B). Due to the increased group size and fissioning, troop A extended their range to include suburbs of Kyoto. This quickly became an irritation to residents and it was decided that a new home had to be found for some of the monkeys. In 1972, troop A of the 22

Arashiyama monkeys was transported to a sanctuary in Texas, where they became known as the Arashiyama West colony (Fedigan and Asquith 1991; Pavelka 1993).

The sex ratio in this species varies, and does not appear to relate directly to provisioning. Furuya (1957) describes an imbalanced sex ratio in Japanese macaques in the wild during his study at the provisioned site of Takasakiyama, with 150 males to 200 females. However, Maruhashi's (1981) study of an unprovisioned group also reveals a skewed sex ratio, with 12 males to 35 females, many of which were juveniles. Sugiyama

(1976) maintains that a sex ratio of one male to four females is not unusual, while Wolfe

(1979) reports a normal sex ratio of one male to two females. Clearly, there is much variation in what is considered the normal sex ratio for this species.

Difficult as it may be to determine the natural sex ratio, an unbalanced ratio can lead to interesting behavioral dynamics. Wolfe (1979) notes that a skewed sex ratio may influence the occurrence of female homosexual behavior in Japanese macaques. Though this behavior is frequently observed in the wild, it appears to occur more frequently with a shortage of male macaques (Wolfe 1979). For example, the Arashiyama West troop of

Japanese macaques is characterized by a higher percentage of females than males. During

Wolfe's (1979) comparison of the sexual behavior of this troop to wild Japanese troops she found that a higher occurrence of female homosexual behavior characterized the West troop.

Though all females regardless of rank participated in the behaviors, low ranking females

more frequently engaged in homosexual consortships (Wolfe 1979). Males have not been

observed to engage in homosexual activities.

The age composition of a wild troop of macaques is very different from the age

composition of captive groups. Furuya (1957) notes that in the wild only half the monkeys 23 studied were adults. Similarly, of 47 unprovisioned macaques at Yakushima Island, 26 were adolescents or juveniles (Maruhashi 1981). However natural a youthful population may be, captive situations are often lacking juveniles and infants completely from their population.

Nakamichi (1984) reports that the age of senility in Japanese monkeys is around twenty years. Though there is much debate over how aging effects female behavior, some researchers seem to agree that senile females, at least in the wild, tend to be less sociable than younger females. Pavelka (1991) notes that this decrease in activity in some females may in fact be influenced more so by the lack of kin groups, and thus social partners, than aging. In her study of free-ranging macaques in Texas she found no evidence that older females, with well-defined kin groups, were less social than younger females (Pavelka 1991).

The relationship between mothers and daughters is key to understanding Japanese macaque society. The troop is composed of matrilineal kin groups that are well associated with a few unrelated central males, and less strongly associated with many peripheral males

(Fedigan 1976). Pavelka (1993:19) emphasizes this point stating, "maternal kin relations hold macaque society together, and guide almost all aspects of social behavior." Like humans, macaques depend heavily on their kin. Females remain with their mother for the remainder of her life, resulting in subsets of related females within the troop (Yamada 1963).

The majority of day-to-day interactions are spent in association with these close female kin

(Pavelka 1993). Those females without kin are very often low-ranked, due to the lack of coalition support, and often spend most of their time alone (Pavelka 1993). Life for male

Japanese macaques though is very different. Most male Japanese macaques only remain in their natal subgroup until adolescence, at which time they typically emigrate out of the troop

(Fedigan 1976). Males typically spend much more time alone than females and generally are 24 not in the company of their female kin. Even those males who do not transfer to another group at maturity do not spend a considerable amount of time socializing with kin (Pavelka

1993).

A stable linear dominance hierarchy also characterizes Japanese macaque society.

Dominance is defined the property of those animals that displace another animal for a certain resource (Pavelka 1993). Dominant animals are privileged within the group, receiving priority access to food, grooming and shade. Dominance and an individual's rank in the hierarchy are determined by alliances that are held together through kinship (Pavelka 1993).

Female Japanese macaques inherit their rank from their mother, occupying a position just below her in the hierarchy. The rank of siblings often follows the "youngest ascendancy" model with the youngest sibling holding the highest position of rank below the mother

(Kawamura 195 8). This "youngest ascendancy" model is important, as it predicts that mothers will always support their youngest offspring before supporting other older offspring.

Males and females have separate dominance hierarchies that are determined by different rules. Male Japanese macaques have a much more difficult time establishing their rank, as most leave the natal group at adolescence. Emigrating males often join nearby troops, which may include older brothers or past acquaintances. New males must then struggle for their rank status in the new troop. Their increase in rank up the dominance hierarchy is both due to opportunities and an individual's personality and ability for planning, intelligence and finesse (Pavelka 1993). Just as each female in the female dominance hierarchy has a rank relative to all other females, so does each male in regard to other males. A dominance relationship also exists between the two hierarchies, with the alpha male always dominant to the alpha female. The entire male hierarchy, though, is not dominant to the entire female 25 hierarchy. For example, a low ranking male is considered subordinate to ahigh-ranking female. Pavelka (1993) notes that even though the alpha male is dominant to the alpha female, his position as alpha depends on her support. The alpha male is only able to ascend to his position by creating alliances and coalitions with other members of the troop. Unlike the alpha female, his position of power is always in jeopardy of being lost if the alliances are not maintained (Pavelka 1993).

Frisch (1959) discusses how the rank order and dominance hierarchy of Japanese macaques can be linked to mounting behavior. It is often observed that the mounting positions of the male and female are switched, with the female or another male taking the mounting position and the male being mounted. This behavior is not thought to be related to sex, but instead functions as an expression of dominance. The animal being mounted is thus subordinate to the other. He notes that, "apparently this behavior serves constantly to re- emphasize the rank order and to make the whole group recognize and support the dominance hierarchy" (Frisch 1959:588). Lunardini's (1989) research with captive Japanese macaques correlates well with this conclusion. In his study, which attempted to classify relationships among the animals, Lunardini (1989) found that the lowest ranking females frequently received the most mounts.

As important as rank and dominance are in Japanese macaque society, this feature alone is not enough to explain all behaviors. Fedigan (1976:9} points out that "dominance- related behavior is only one of a characteristic set of behaviors attributable to an individual as a functioning member of his group." She also notes that other factors that may influence wild Japanese macaque behavior include temperament, age, sex, kin group, and past history. 26

Thus, it must be remembered when studying these primates, that as important as rank is, clearly there are other factors at play in the society as well.

All primates are known for their concern with grooming. Grooming performs the function of removing ecto-parasites and helps to maintain social bonds between individuals.

Most primates are social animals; thus this latter role is very important to the stability of the group (Carpenter 1942). Grooming is a way of forming affiliative relationships between animals in the group and as a way to strengthen and maintain the dominance hierarchy.

Furuya (1957) detailed grooming in wild Japanese macaques. A grooming session might be initiated with one macaque presenting a body part to another, thus soliciting another to groom. During grooming, Furuya (1957) noted that the back was the body part most often groomed, with bare skin areas rarely groomed and objects found in the hair eaten. In general, the grooming behavior began after feeding was finished in the morning, steadily increased throughout the day as temperatures increased and dropped in frequency as temperatures decreased (Furuya 1957).

Seyfarth (1977) noted the importance of grooming and rank in primates in his model predicting female grooming behavior. He predicted that females will compete to groom the highest ranking females (Seyfarth 1977). This behavior results from the desire to create powerful coalition partners. This competition to groom higher ranking animals should result in most grooming occurring between adjacently ranked pairs (Seyfarth 1977). Though this hypothesis is supported for some species, including vervet monkeys (Chlorocebus aethiops), it is not supported for others such as rhesus macaques (M. mulatta) (Matheson and Bernstein

2000). Rhesus macaques are similar to Japanese macaques in that they also live in hierarchical societies. Though data have not yet been found to disprove this idea in Japanese 27 macaques, the lack of support of the model for rhesus macaques suggests it may not be appropriate for Japanese macaques.

Research on many macaque species supports the assumption that grooming is related to coalition planning. Mayagoitia et al. (1993) found an increase in grooming prior to feeding in captive stumptail macaques (M. arctoides). These authors concluded that the frequency of grooming increased in order to secure coalitions, which may be necessary during feeding (Mayagoitia et al. 1993). Henzi and Barrett (1999) reject this position, noting that coalition formation is better explained by the desire to improve one's rank than to short- term access to resources.

An alternative interpretation is that grooming may be more important in maintaining

social harmony within the group. Kapsalis and Berman's (1996) study of captive rhesus

monkeys suggests that grooming is more important in promoting social tolerance rather than

in creating coalitions. Stammback and Krummer (1982) also note the importance of

grooming in the maintenance of relationships in hamadryas baboons (Papio hamadryas

hamadryas). Additionally, reconciliation, which is the affiliative reunion between

aggressors, has often been observed in primates and often takes its form through grooming

(de Waal and Aureli 2000).

Though there appears to be much discussion in the literature over the function of

grooming in primates, there is no one function to this behavior. Whether to maintain

dominance hierarchies, create coalitions, maintain social bonds, or to reduce tension,

grooming is clearly a key characteristic of many primate species. 28

Summary

Japanese macaque society is similar to human society in that it is incredibly complex.

Life for these primates is full of complex interactions and is guided by a stringent dominance hierarchy. These interactions and the resulting dominance hierarchy are species-specific to the Japanese macaque. In order to maintain the behavioral complexity characteristic of the natural environment, it is crucial that these behaviors be maintained under captive conditions.

Naturalizing the enclosure, adding enriching foods and stimuli, and allowing kin relations through the formation of matrilines, will aid in maintaining the physical and psychological well-being of this species.

The zoos examined in this study can be expected to support some aspects of the species-specific repertoire of wild macaques for several reasons. Both zoos are naturalistic enclosures, natural stimuli such as trees, vegetation and water are available. However, both zoos can be characterized as having a lack of novel items to stimulate the monkeys, in that enrichment activates are basically non-existent. This may result in a decrease in time spent active in their environment. Additionally, the social environment of the zoo, with non-varied social partners, and small kin groups may impede the development of social relations, through affiliative behaviors, as one would expect in the wild. Only through examining these possibilities for difference between wild and captive populations can it be understand how the habitats can be altered to be more beneficial to the animals. 29

CHAPTER 3. METHODOLOGY

Subjects and Study Sites

This study was conducted on two troops of captive Japanese macaques housed in zoological parks. One group of fifteen macaques was studied at the Minnesota Zoo, in Apple

Valley, Minnesota. The second troop studied included twenty-one macaques at the Blank

Park Zoo, in Des Moines, Iowa.

The Minnesota troop consisted of fourteen females and one male. The zoo originally acquired macaques, from which all current females are descended, from the Texas Snow

Monkey Sanctuary. The females can be divided into the matrilines Betta, Rheus, Nose, and

Rotte. The Rheus matriline is further divided into two groups, A and B. Personnel at

Minnesota are unaware of how the two Rheus groups are related; only certain they are descendants of the Rheus matriline from Texas. Table 3.1 summarizes basic information on the troop, including individual names, identification number, birthdate, age during study, kin relations, and discrete physical characteristics. The only male, Nikko, is not known to be related to any of the females. Nikko is a newer arrival to the troop, acquired by the zoo in

2001. He was obtained as a breeding male, but two years have passed with no resulting pregnancies. An examination revealed that he was sterile. The zoo performed surgery on him to remedy the situation. Examinations since the surgery have shown he is capable of producing sperm. Currently though, the troop only consists of adult macaques, and none of the females are known to be pregnant at the time of study. The macaque exhibit at

Minnesota consists of two enclosures: an outdoor exhibit for zoo operating hours and an indoor exhibit used when the zoo is closed. The monkeys are held in an approximately 3,300 30

Table 3.1. Description of Japanese macaques at the Minnesota Zoo Birth Age Physical . Kin Group Name I.D. Kin Relations Year (yrs) Characteristics

Nikko* 10097 1983 20 N/D** Offspring: Betta Anna 2978 1982 21 Blond hair Margie Margie 6178 1989 14 Missing hair

Nikki 6492 1990 13 Aunt: Anna N/D** Overweight, Nose Mary 3010 1982 21 Sibling: Missy missing hair Missy 5168 1987 16 Obese Offspring: Limp, scar on Rheus A Boo 1756 1980 23 Heather back Ellen 3 844 1984 19 Missing hair

Heather 6896 1991 12 N/D** Offspring: Rheus B Babs 3791 1984 19 Obese Doris, Flo Doris 4358 1985 18 Missing hair

Flo 5131 1987 16 Small Offspring: Rotte Liza 4412 1985 18 Missing hair Susie, Sara Susie 6123 1989 14 N/D *

Sara 6940 1991 12 Large * Male ** N/D indicates no obvious describable physical characteristics

Figure 3.1. Enclosure at the Minnesota Zoo 31

square meter outdoor enclosure from approximately 9:00 a.m. — 6:00 p.m. (Figure 3.1). The exhibit is enriched with trees, rocks, living vegetation, freshwater pools and steams. In addition, the exhibit is enriched with food. Every morning softened peas and sunflower seeds are scattered throughout the enclosure. Two days a week an additional food treat is hidden in the exhibit. A four meter high stone perimeter wall surrounds the exhibit. This wall is not a usable climbing surface for the monkeys. Visitors view the monkeys by looking down into the enclosure or through the Visitor Center overlooking the exhibit. The Visitor

Center hangs over the exhibit by at least three meters, creating shelter for the monkeys.

Several large poles located next to the perimeter wall also give the macaques opportunities to partially hide from the visitors if they choose.

The monkeys are held in the indoor enclosure during non-operational hours. The

indoor exhibit consists of five interconnected rooms with sleeping boards. The size of the

rooms varies, but the total space is approximately 188 square meters. Monkeys are fed a primate maintenance diet while in the indoor exhibit, consisting of a monkey biscuit made by

Mazuri feeds. The entire troop receives approximately 2.72 kilograms of biscuit each evening. In addition, they receive 5 00 grams of Marion leaf eater biscuit, 600 grams of carrot and eight oranges while in the indoor facility.

The Blank Park troop consists of 21 individuals, of which 16 are females and five are

males. As at Minnesota, all of the monkeys are adults. The colony is considered anon-

breeding facility due to breeding control measures. All males have either undergone a

vasectomy or have been castrated. The monkeys can be classified into six groups, five of

which are composed of related kin. All of the monkeys except for one (Big Belly) have 32

Table 3.2. Description of Japanese macaques at the Blank Park Zoo Age Physical Kin Group Name I.D. Birth year Kin Relations (yrs) Characteristics Offspring: A Fro 139 1976 27 Limey, Smee, Blondish hair Sam Back legs bent, Limey 305 1986 17 limps Missing hair on Smee 662 1990 13 neck Sam* 847 1991 12 NlD** Siblings: B Merry* 494 1988 15 Binky, Bilbo, N/D** Pale Binky 592 1989 14 Overweight

Bilbo* 833 1991 12 N/D**

Pale* 1204 1995 8 N/D** Offspring: Ole, Limps, white hair, Baldy 142 1974 29 Blue, Toto, C balding on head Norma, Lena Offspring: N1D** Ole 321 1986 17 Tinker Blue stripe visible Blue 489 1988 15 on belly, obese Toto 598 1989 14 Overweight One enlarged Norma 790 1991 12 nipple Small, broken Tinker 864 1991 12 p~Y Lena 1208 1995 8 Small

D Big Belly 147 1985 18 Obese Offspring: E Shera 144 1982 21 Blondish hair April, Pippin Growth on right April 441 1987 16 thigh Pippin* 644 1990 13 N/D**

F Gizmo 861 1991 12 Sibling: Tres Overweight

Tres 1196 1995 8 Small

* Male ** N/D indicates no obvious describable physical characteristics 33 either mothers, siblings or both within the troop. Table 3.2 describes the Blank Park macaques, including kin relations, birthdate, zoo identification number, and physical characteristics.

Names of individuals and kin groups were not available at Blank Park, so names were given to facilitate data collection. All monkeys were born at Blank Park with the exception of Baldy, Fro and Shera. Baldy and Fro were born at the Texas Snow Monkey Sanctuary, transported to Minnesota, and sent to Blank Park in 1985. Shera was born at Minnesota and was also sent to Blank Park in 1985.

Figure 3.2. Enclosure at the Blank Park Zoo

Blank Park houses the macaques in an outdoor exhibit from 9:00 a.m. — 5:00 p.m. and in an indoor exhibit when the zoo is not operational. The outdoor enclosure is approximately

975 square meters (Figure 3.2). This enclosure is enriched with a number of pools, trees, rocks, logs and ropes. In addition, the enclosure is a cage design, allowing the monkeys to climb up the cage and onto the wire ceiling if they desire. The cage also includes ledges for climbing and a pole to slide down. Visitors can view the monkeys on all sides of the enclosure, though there is one location inside the cage that allows the monkeys to hide from 34 visitors. This site is a hollow with a flap over the cover. Freshwater can be retrieved from any of the pools and also from a water tap (lixit). Monkey biscuit (approximately 2.25 kilograms), various types of fruit, and peas are spread throughout the outdoor enclosure

before the monkeys are released for the day. Occasionally, a seed mix is also scattered throughout the cage at mid-day. Once or twice a week, usually during the summer months, the monkeys are given fruit cubes (raisins frozen in water cubes) around mid-day. During a few observations, when monkeys at Blank Park were fed during a focal session, the excitement of feeding led to a loss of the focal animal and observations were halted. During one observation period, two balls were thrown into the exhibit area for extra enrichment.

The macaques are held in the indoor exhibit during non-operational hours. This exhibit consists of five interconnecting rooms that total approximately 275 square meters.

During the evening hours the monkeys were fed approximately 2.25 kilograms of monkey

biscuit. Additionally, various food enrichment is added to the rooms, including peanuts,

seeds or hay in a puzzle box or in a log hollow. Parrot mix, trapper peas, and alfalfa hay are

also spread throughout the rooms. The indoor facility includes swings, branches, ropes and

fire hoses. Various toys such as Boomer ballsTM, Fortex tubsTM, and KongTM toys are also

given periodically.

Data Collection Methods

The data for this study were collected during the non-breeding season, between the

months of May and September 2003. Data were collected at Minnesota from May 13 -June

17 and at Blank Park from June 21 -August 22. Monkeys were observed at both zoos

between 9:00 a.m. and 4:30 p.m. Four hours of observations on each monkey were collected

in 15-minute continuous focal sample periods. Attempts were made to randomize the time of 35 day and order of individual focal samples. Focal animal sampling, based on procedures outlined by Altmann (1974), was used to record behavioral states and events. Paterson (2001) defines an event as a momentary behavior for which duration is not recorded. He defines a state as any behavior that can be measured. The duration of activity was recorded to the hundredth of a second for states.

Ad Libitum sampling methods, as described by Altmann (1974), were also employed for observations. Whenever possible, behavioral observations were recorded on non-focal monkeys, as long as this did not draw attention away from the focal monkey. These data, following a procedure outlined by Appleby (1984), were used to construct the dominance hierarchy for individuals at both zoos (Tables 5.7-5.9).

All data were entered into Microsoft Excel. The categories analyzed were broadened to include behavioral states, which entailed classifying such events as jump and drink into larger behavioral categories. An ethogram, modified from Fedigan (1976), was used to record behaviors for agonism, allogroom, autogroom, feed, inactivity, move, object manipulate, play and sexual activity (see Appendix for ethogram).

Analysis

Analyses focused on two main questions: how is behavior at Blank Park and

Minnesota different/similar and how does the activity budget of captive macaques resemble or differ from wild monkeys? Analyses included both non-social and social behaviors.

Non-social behaviors reflect time spent inactive, moving, feeding, auto-grooming and manipulating objects. Social behaviors include allogrooming, play, sexual behavior and agonistic behaviors. 36

Data were analyzed using Microsoft Excel for Windows. The conditional sum operation was used to determine the total amount of time engaged in each activity per focal period. The data were than analyzed using a single factor Analysis of Variance (ANOVA).

The ANOVA test was used to compare zoos. The null hypothesis was that no difference between the zoos would be detected. The alternative hypothesis was that zoos differ regarding subjects' activity budgets. Significance level was set at 95% so that p-values less than 0.05 were considered statistically significant and were evidence to reject the null hypothesis. ANOVA depends on the assumption that the data are normal (Madrigal 1998).

Therefore, the first step was to use exploratory data analyses (descriptive statistics and histograms) to reveal any abnormalities within the data. Descriptive statistics revealed that for most behavioral categories, the data were not skewed. However, the data were skewed for object manipulation, play and sexual activity, each of which occurred at very low frequencies. Thus, these data were not considered to be normal and ANOVA was not used to analyze these three categories.

The dominance hierarchy was constructed by summing all observations of displacements and other agonistic encounters into a dominance matrix (Table 5.7-5.9). To determine whether grooming patterns reflected kin ties, only simple tabulations were made due to the small sample size.

Results were compared to Maruhashi's (1981) study of the Ko-troop monkeys on

Yakushima Island, Japan. This study was chosen for several reasons. This is one of the few sites in Japan where monkeys have not been provisioned with food. The monkeys at this site live in a warm, temperate forest. The yearly average temperature is 20° C (range 11°-3 0°).

This is comparable to temperatures during the present study. The average temperature at the 37

Minnesota site during the study months was 17.5° C. In Des Moines, the average temperature during data collection was 23.3° C. Both values lay well within the range of temperatures observed at Yakushima. The lack of provisioning is reflected in the group size of monkeys found on this island compared to other sites where monkeys are provisioned.

Ko-troop was composed of 47 members: three adult males, nine juvenile males, eighteen adult females and seventeen juvenile females. This ratio of adult males to adult females is comparable to that found within each zoo studied here. Most importantly though, Maruhashi

(1981) created activity budgets for each age and sex category, something that was not found for other sites where Japanese macaques have been studied. Hence comparisons can be made specifically to captive and wild adult males and females. There are a few problems with comparing to Ko-troop however. The macaques on this island are classified as a different subspecies, M. fuscata yakui, than the present study, M. fuscata fuscata. However, this may not be problematic, since researchers are not in agreement as to whether this separation of the species is accurate (Nozawa et al. 1991). Another problem that exists when comparing these monkeys is that Maruhashi (1981) collected the data between the months of August and

December. A portion of this time includes the mating season, which is normally between

September and February. Maruhashi's (1981) study also lumps several of the less prominent social behaviors: play, sexual behavior, and agonism, into an "other" category.

Unfortunately, lumping these very different social behaviors into one category does not make comparing frequencies between the captive and wild macaques conducive. Therefore to analyze the data for these behaviors other means of comparison from the literature were used. 38

CHAPTER 4. RESULTS AND DISCUSSION: NON-SOCAL BEHAVIORS

Non-social behaviors are a major part of the activity budget of both wild and captive

Japanese macaques. These behaviors also account for the majority of all activity of the captive macaques in this study (82 % of time). Non-social behaviors include time spent inactive, moving, feeding, manipulating objects, and autogrooming. Figures 4.1 and 4.2 display the percentage of time spent in non-social activities by individuals at Blank Park and

Minnesota respectively. Figures 4.1 and 4.2 show that individuals vary regarding the amount of time engaged in the various categories. This variability will be discussed in the following sections.

loo ■ Autogroom 90 - ®Feed Inactive 80 - ■Move Manipulate 70

~ 60 -

50 - U ~,

a 40 J w

30 -

20 -

10-

0 I I ~~~ i

Subject

Figure 4.1. Percentage of time spent in non-social behaviors at the Blank Park Zoo 39

100 90 - ■ Autogroom ■Feed 80 - Inactive 70 - ■ Move Manipulate 60 -

50 - U s.. a 40 -

30 - _

20 -

10-

fifi~ b~ 4' ~

Subject Figure 4.2. Percentage of time spent in non-social behavior at the Minnesota Zoo

Inactivity

Most monkeys in the study spent the majority of their time in an inactive state.

During inactivity periods animals usually were sitting up and often looking either at visitors or other monkeys. They were also seen lying down, or resting, but attempts were not made to distinguish between these categories. At Blank Park, many individuals spent their time inactive holding onto the wire of their cage and looking out. At Minnesota, individuals were not observed being inactive in any certain location. It appeared that certain macaques had preferable spots in which to sit, but the data were not collected systematically.

As Figures 4.1 ;and 4.2 show, inactivity levels vary between monkeys. Inactivity among monkeys at both zoos ranges from 17% to 65% of the total time budget with a mean of 43%. For 29 of the 36 monkeys in the study, inactivity was the most prominent behavior.

Thirteen of the 36 individuals spent more than half of their total time budget inactive. At 40

Blank Park, 43% of monkeys spent more than half of their time inactive, while at Minnesota this figure was only 27%.

Table 4.1. Comparison of time spent inactive Subjects Percentage All Monkeys 42.6 Blank Park 45.6 Minnesota 38.5 All Males 46.1 All Females 41.9 Blank Park Females 44.5 114innesota Females 38.9

Table 4.1 summarizes the percentage of time spent inactive for monkeys in the study.

Males were not distinguished by zoo due to the uneven ratio (one male at Minnesota verses five at Blank Park). Monkeys spent 45.6% of time at Blank Park and 38.5% of time at

Minnesota inactive. This difference was not statistically significant (ANOVA: df =1; p=0.104). The amount of time spent inactive by males was slightly higher, 46.1%, than the inactivity levels of females, 41.9%. Blank Park females appear slightly more inactive than those at Minnesota, with inactivity level of 44.5 % and 38.9%, respectively. It should be noted that the range of inactivity varied by 48% between individuals at Blank Park, and by

32% at Minnesota.

Table 4.2. Percentage of time budget spent inactive by captive and wild macaques Site Females Males) Yakushima 18.4% 35.3% Blank Park 44.5% 48.9% Minnesota 38.9% 32.3% Zoo Average 41.9% 46.1

Table 4.2 compares the inactivity level of captive and wild Japanese macaques. In general, for both males and females, captive monkeys spent more time inactive than wild monkeys. At Minnesota, Nikko was actually found to spend less time inactive than wild monkeys; however, the overall inactivity for all males is greater than wild monkeys (46.1 41 and 35.3 %respectively). The comparison between captive and wild females was much more extreme. At both zoos females were much more inactive than their wild counterparts, with the inactivity level for both zoos being 23%greater than wild monkeys.

Discussion: Inactivity

Inactivity preoccupies the bulk of the time of both males and females at each zoo.

This study supports some observations regarding the inactivity level characteristic of

Japanese macaques and is inconsistent with others. Both zoos appear similar in time spent inactive, with the most prominent difference regarding inactivity being between captive and wild macaques.

Studies have noted that males spend more time inactive than females (Maruhashi

1981). This was true in captivity, with males inactive 46.1%and females 41.9%. However, the difference between males and females in captivity is not nearly as extreme as that observed among wild monkeys at Yakushima (Maruhashi 19.81). For wild male macaques, inactivity is the predominant part of their daily life, with Yakazuri males spending 35.3 % of the day inactive (Maruhashi 1981); hence, it is not unnatural that captive male macaques spent a large portion of their day inactive as well. However, wild females spend only 18.4% of their day inactive (Maruhashi 1981). Other sites throughout Japan also report fairly low inactivity rates (Yotsumoto 1979). Clearly, it is atypical that captive females spend approximately 42% of their day inactive.

This study contrasts with work by Hauser and Tyrell (1984) who examined inactivity in older female Japanese macaques. They found that old females were less active than younger females. The oldest individuals in this study, Boo, Baldy, Fro and Shera are not among those that spend most of their time inactive. Pavelka (1991) describes how the notion 42

that old females are more inactive than others is inaccurate. Old females may be more likely

not to have any female kin remaining in their group. If this were the case they would lack

constant social partners. She observed that females without social partners tended to be more

inactive (Pavelka 1993). All of the older females in this study, however, have well-defined

kin groups, which probably explains why they were not observed to be particularly inactive.

Move

Movement at both zoos typically consisted of walking. Monkeys at both zoos were

also observed to climb trees, logs, and the cage wall (at Blank Park only). Running was

occasionally observed, as was swimming.

Time spent moving did not vary as much between individuals as did time spent being

inactive (Figures 4.1 and 4.2). Monkeys at Blank Park spent from 3.8% - 16.9% of their time

moving. The range at Minnesota was similar, with 5.7% to 16.9% of the time budget spent

moving. Only one monkey, Baldy, spent less than 5% of her total time moving.

Table 4.3. Comparison of time spent moving Subjects Percentage All Monkeys 10.7 Blank Park 10.4 Minnesota 11.1 All Males 8.9 All Females 11.0 Blank Park Females 10.6 Minnesota Females 11.5

Table 4.3 describes the percentage of total time spent moving by monkeys over the course of the study. These values appear to be similar across groups, though males did move less than females. When the data were analyzed to observe differences between zoos, no significant difference was found (ANOVA: d~l;p=0.523). 43

Table 4.4 compares time spent moving between wild and captive monkeys at each zoo. Time. spent moving for wild macaques is approximately twice that of captive monkeys.

Captive macaques moved 11.0% of the time budget for females and 8.9% for males. This is very different from the values of 20.5% for females and 17.9% for males at Yakushima.

Table 4.4. Percentage of time budget spent moving by captive and wild macaques Site Females Males) Yakushima 20.5% 17.9% Blank Park 10.6% 9.6% l~tinnesota 11.5% 5.7% Zoo Average 11.0% 8.9%

Discussion: Moving

Yotsumoto (1976) distinguishes between two types of moving for wild Japanese macaques: rapid transport of the troop to different areas within their range, and movement within the area where the troop has stationed itself. Clearly comparing between wild and captive monkeys is problematic, regarding the former. Captive animals will only have opportunities to move around their cage. This probably accounts for most of the difference observed between wild and captive monkeys, as wild monkeys have others areas of their range to explore while captive monkeys do not.

Feeding

Observations of feeding between zoos differed, mainly in type of food collected.

Minnesota monkeys did not have monkey chow available in their outdoor enclosure, so could not be observed to feed on this material. However, they were often seen foraging through the grass and rocks, possibly for scattered peas. Monkeys at Blank Park were observed to feed regularly on monkey chow and scattered fruits. Individuals at both zoos were observed to eat grasses. 44

Table 4.5. Comparison of time spent feeding Subjects Percentage All Monkeys 15.7 Blank Park 11.3 Minnesota 21.8 All Males 14.1 All Females 16.0 Blank Park Females 11.2 Minnesota Females 21.5

Figures 4.1 and 4.2 illustrate the high degree of feeding variation among monkeys.

Time spent feeding ranges from 2% to 43% of the total time budget, and appears to differ between the two zoos. As is seen in Table 4.S, the time spent feeding at Minnesota was

21.8% of the total activity budget (range 3-42%). At Blank Park, 11.3% of the total time budget (range 2-21%) was spent feeding. Analyses revealed that the difference observed between zoos was significant (ANOVA: df=1; p=0.033).

Table 4.6. Percentage of time budget spent feeding by captive and wild macaques Site Females Males) Yakushima 24.8% 15.9% Blank Park 11.2% 11.8% Minnesota 21.5% 25.5% Zoo Average 16.0% 14.1

Table 4.6 compares the percentage of time spent feeding between captive and wild

Japanese macaques. Minnesota females are very similar in their feeding habits to wild females at Yakushima, feeding 21.5% of the time compared to the wild monkeys' 24.8%.

Females at Blank Park, however, fed considerably less, engaged in feeding only 11.2% of the time. At Minnesota, Nikko actually fed more than wild males, while, at Blank Park, the males fed slightly less than the Yakushima males. Time spent feeding for all captive males in the study is similar to wild males. The average amount of time spent feeding by captive females, though, is very low due to the low amount of time spent feeding at Blank Park. 45

Discussion: Feeding

These results regarding time spent feeding are interesting in that they seem contrary to what one would expect given the environmental conditions. Blank Park monkeys foraged less despite the obvious plentitude of food. They are fed a food ration in the morning, and it is available to them all day, contrary to Minnesota where their main diet of monkey biscuit is only available in the holding area. At Blank Park, the monkeys do not need to search for their food. They can find their food faster, in large pieces. Additionally, the Minnesota monkeys have an enclosure nearly double the size of Blank Park. This may increase the required time to find suitable food. The result though, that Minnesota macaques spend more time foraging than Blank Park monkeys, is not proof that either group eats more than the other. It simply shows that at Minnesota, monkeys spend more time actually looking for food. It seems significant that at Minnesota, the biscuit is not available in the outdoor enclosure. This forces the monkeys to search for the scattered peas. This strategy could be beneficial to the Blank Park macaques. Additionally, Reinhardt and Roberts (1997) discuss several feeding enrichment strategies that may help to increase foraging time for macaques at

Blank Park. In their study they found that the most effective feeding enrichment strategies either involved feeding the animals whole, unprocessed foods, or using some type of puzzle feeder to feed biscuits (Reinhardt and Roberts 1997). Both types of enrichment would force the monkeys to work for their food rather than simply picking it off the ground.

A notable difference between zoos is the occasional extra feeding of macaques at

Blank Park. On some afternoons, Blank Park monkeys were fed an extra treat. In the summer, this usually consisted of some kind of frozen fruit treat. In Waitt and Buchanan-

Smith's (2001) study of captive stump-tail macaque (M. arctoides) behavior they discuss 46 possible behavioral outcomes of anticipated feeding. Predictable occurrences such as feeding actually decreased stress levels in captive animals (Want and Buchanan-Smith 2001). They observed that when feeding was late or delayed, animals spent time in anticipation of feeding and were more likely to engage in abnormal behaviors and agonism, and were less likely to engage in affiliation. Abnormal behaviors were not observed at Blank Park, although, monkeys did appear to be anxious when keepers passed (emitting vocalizations and climbing cage walls), seemingly in anticipation of food. During feeding, agonism between monkeys was higher, though it was not possible to acquire a precise estimate of rate of occurrence due to the excitement among monkeys. Waitt and Buchanan-Smith (2001) note that other studies have found that feeding captive primates on highly unpredictable schedules may be beneficial. This type of scheduling would not allow the animals to expect feeding at any certain time, thus decreasing tension within the group and within individuals. In this regard, the extra feedings during midday at Blank Park can be considered unpredictable. They did usually occur after noon, but it was not a daily occurrence. This may be why abnormalities were not observed within the troop around possible feeding times.

Figure 4.3. Big Belly at the Blank Park Zoo 47

Both zoos have several monkeys that can be considered obese. At Minnesota, Missy and Babs appear obese, as do Big Belly and Blue at Blank Park. Though the exact weight of the monkeys is unknown, all have very large bellies (Figure 4.3 ). Personal communication with the keepers has also verified these monkeys as obese. One would have expected these obese monkeys to spend more time feeding. However, Big Belly, Blue, Babs, and Missy did not feed an exceptionally high amount, with feeding percentages of 2%, 8%, 19.5%, and

15%, respectively. These values are well below the natural time spent foraging at

Yakushima (Maruhashi 1981). However, this is not evidence that any of these monkeys eats less than other individuals. Feeding activity is often time spent actively walking around and looking for food. A low foraging percentage simply means that these monkeys did others things with their time. As Figures 4.1 and 4.2 display, three of these monkeys, Big Belly,

Blue and Babs spent very large amounts of time inactive. To get their nutritional requirement, perhaps they ate larger amounts of food more quickly, or ate more high-energy food than other monkeys. At Minnesota, it is particularly difficult to determine how much each monkey was eating since the main feeding of the monkeys was in the indoor exhibit and was not observed.

Studies of many primate species in the wild have shown that males tend to spend less time foraging than females. Glutton-Brock (1977) observed three reasons for this tendency:

1) males do not incur the energy cost of feeding and lactation; 2) they are often dominant to females and maintain access to areas where food supply is most abundant and 3) they often feed faster than females. This study does not seem to support these explanations, at least when comparing between males and females within zoos. There does not appear to be any

large difference in time spent feeding. However, as there is only one male at Minnesota, it is 48 not valid to make any conclusions based on Minnesota monkeys. Also, at Blank Park, it appears that the females simply fed at an abnormally low rate when compared to the other samples. In comparison to wild populations, the Minnesota females and the average value for males at both zoos reflect Glutton-Brock's (1977) observations, with feeding values of

21.5 %and 14% respectively. Clearly, however, the reasons for why males forage faster than females is not due to female lactation or pregnancy at either zoo. Male domination of food was also not observed. Thus, the chances are good that males simply eat faster than females.

This at present is only a hypothesis, since data were not collected in a manner that can evaluate this assertion.

Making a strict comparison of feeding behavior between wild and captive monkeys is problematic. Monkeys in the wild have food available to them in many different ways.

Depending on the season, food may be abundant or scarce. Seasons will not often affect feeding in zoos. Food will always be available and it will be predictable regarding where, what and approximately when monkeys will receive it. In addition to wild macaques' feeding being highly variable, Yotsumoto (1976) explained that at some Japanese macaque sites, feeding is mainly an arboreal behavior. This species-specific behavior could not be observed at either zoo. Time spent in the trees was mainly for resting and grooming.

Occasionally, macaques would bring a monkey biscuit into the tree, but they never had opportunities to actually feed from trees since the trees at both zoos did not offer any edible vegetation.

Ubject Manipulation

Object manipulation was noted whenever monkeys were handling an object, but not eating it. At Minnesota, object manipulation mostly consisted of biting or handling objects 49 that had fallen into their exhibit. These included plastic bottles, shoes, paper, plastic bags, and other garbage. At Blank Park, garbage was never seen within the exhibit, as visitors were not observed to throw materials into the cage. This was probably due to the different exhibit structures. Visitors at Blank Park would have to throw an object several feet through the wire and into the cage versus simply dropping an object over the perimeter wall at

Minnesota. Additionally, monkeys at Minnesota were often found sitting at the base of the perimeter wall, looking up at the visitors, which may have encouraged people to drop objects or food. Also, at Blank Park, there are signs instructing visitors not to throw items to the monkeys. These signs were not present at Minnesota. Object manipulation at Blank Park often involved picking at or licking the wire of the cage. In particular, there is a black layer of paint peeling off of the cage that monkeys removed. Object manipulation at both zoos involved picking at bark and moving logs.

Two events in particular stand out in terms of object manipulation at Blank Park. The first occurrence on a day in which two plastic balls were added to the exhibit as enrichment, and the second event occurring on a day when a bird had become trapped in the cage.

Because of the nature of the Blank Park exhibit, it is possible for birds to get into the cage, but they may not be able to escape if they are panicked. On August 13~ a mourning dove became trapped in the cage, and some of the monkeys became preoccupied with it. What is striking about this example is that there was no intention to eat the bird for the first hour of the bird's capture. Sam, the dominant male, was the first to take possession of the bird.

Rather than eat it, he simply sat with it in the tree, roughly holding its wing, while the bird struggled to escape. He later dropped it and lost interest. At this point Lena took the bird and began dipping it in one of the pools. She proceeded to rub the still living bird on the 50 rocks near the pool, occasionally stopping to dunk the bird in the water. In the entire course of her manipulation of this bird, she did not once bite it. It was not until Pippin took the bird, one hour after its capture, that feeding was observed. At this point the bird was dead and

Pippin was clearly ingesting some of the bird. These observations were collected in the morning when plenty of monkey chow and random fruits were still available.

On another occasion, two plastic balls were thrown into the exhibit; again the monkeys that possessed the objects were Sam and Lena. The monkeys treated the balls very similar to their treatment of the bird; Sam simply sat with it, and Lena rolled it in the water on the rocks. Both cases only involved a few monkeys and did seem to increase both tension

(agonism between monkeys for the object) and activity (actively manipulating the object).

The tension observed, though, did not escalate into physical violence; in fact, reconciliation was observed after some agonistic encounters.

Table 4.7. Comparison of time manipulating objects Subjects Percentage All Monkeys 1.4 Blank Park 1.7 Minnesota 1.1 All Males 1.0 All Females 1.5 Blank Park Females 1.8 l~Zinnesota Females 1.2

Object manipulation represented a very small amount of individual time budgets. As

Figures 4.1 and 4.2 show, not all monkeys were observed to exhibit this behavior. Only two individuals engaged in object manipulation more than S % of their time. These monkeys,

Lena (8%) and Tres (6%) are both from Blank Park. As Table 4.7 shows, object manipulation only consisted of 1.4 % of the total time budget for all monkeys in the study. 51

Females were found to spend slightly more time engaged in this behavior (1.5%) compared to males (1%).

Between zoos, Blank Park monkeys spent a slightly higher percentage of the total observation time, 1.7% (range 0% - 8%), engaged in object manipulation than Minnesota monkeys, 1.1% (range 0% - 4%). However, it is highly unlikely that this is a significant difference. It was not possible to perform analyses on this category due to the non-normality of the data. Both zoos seemed similar in providing opportunities for this behavior, in that unnatural objects (e.g., garbage, balls, cage wire) and natural items (e.g., birds, bark) were available to the individuals.

Discussion: Object Manipulate

Though object manipulation made up a very small proportion of time, it is clear that it is a normal part of the activity budget of macaques at both zoos. Novak et al. (1994:285) describe the curious nature of macaques, which spend "a significant proportion of their time selectively exploring and manipulating stimuli in their natural environment." They note that wild macaques often manipulate stones, bark, dirt and even use tools in food extraction. This natural curiosity often leads to innovations, such as the famous sweet potato washing, which lends itself to being culturally transmitted (Hirata 2001).

Observations of wild macaques have noted a gender bias in the amount of time spent manipulating objects, with females engaged in this activity more often than males (Novak et al. 1994). This observation was also made in this study, though the difference between males and females was not great; with males spending 1%and females spending 1.5% of their time budget engaged in this behavior. Novak et al. (1994) also note that time spent manipulating objects varies among captive groups depending on potential stimuli available. This 52 observation was also supported by the present study, with monkeys at Blank Park spending slightly more time in this behavior than those at Minnesota. Both values, though, are very small, so it is difficult to confirm that Blank Park monkeys engaged in this behavior more than Minnesota monkeys, especially since both troops had plenty of opportunities to engage in this behavior.

This category is closely tied to feeding activity, in that occasionally a behavior that began as object manipulation eventually led to foraging. Bayne et al. (1994) note that objects that increase the likelihood of foraging opportunities and grooming may be more valuable than simple toys to captive macaques. At Blank Park, the manipulation of the bird eventually led to its ingestion. The manipulation of the plastic balls led to more social interactions among the monkeys. In particular, agonism and then reconciliation through grooming were observed during this period. Though it is difficult to find rates on the exact amount of time spent engaged in this activity, it is clear that it is a normal part of the Japanese macaques' daily life.

Autogroom

Autogrooming was observed any time a monkey was seen picking or licking their own skin and hair. This behavior was non-social and was typically seen when monkeys were sitting, either on the ground or in a tree. It was also observed ad libitum, that monkeys tended to autogroom occasionally after agonistic encounters.

Time spent autogrooming varies considerably between individuals. As Figures 4.1 and 4.2 show, autogrooming is typically the third most important activity for monkeys. The amount of time spent autogrooming was 11.2% (range 2.4% - 28.2%) of the total time budget for all subjects in the study. This is representative of values found at the individual zoos, 53 with 11.3% (range 2.4% - 28.2%) at Blank Park and 10.9% (range 3-7% - 20.2%) at

Minnesota (Table 4.8). Analyses did not reveal a significant difference between zoos

(ANOVA: df =1; p=0.844). Clearly the ranges illustrate that there is much inter-individual variation. When males and females were compared, it was found that males spent slightly more time (12.5%) autogrooming than females (10.9%). However, this difference is probably not significant.

Table 4.8. Comparison of the time spent autogrooming by monkeys Subjects Percentage All Monkeys 11.2 Blank Park 11.3 Minnesota 10.9 All Males 12.5 All Females 10.9 Blank Park Females 11.3 Mintlesota Females 10.4

As Table 4.9 summarizes, captive Japanese macaques in this study were found to autogroom much more frequently than wild Japanese macaques. The difference is quite prominent, with Yakushima monkeys autogrooming approximately ten times less than captive macaques. In the wild, males tended to autogroom slightly more often than females, which is similar to results found within each zoo.

Table 4.9. Percentage of time budget spent autogrooming by captive and wild macaques Site Females Male (s) Yakushima 1.2% 1.7% Blank Park 11.3% 11.5% Minnesota 10.4% 17.3 Zoo Average 10.9% 12.5%

Discussion: Autogroom

The amount of autogrooming observed between captive and wild macaques is quite different. Research at multiple sites has reported that this behavior is relatively rare in the

wild (Maruhashi 1981; Kurland 1972). Clearly, though, it is a very prominent part of the 54 captive time budget for monkeys at both zoos. Rosenblum et al. (1966) observed that autogrooming and allogrooming should be inversely correlated with one another, in light of its partial hygienic function. Research by Kurland (1977) supports the presence of this inverse correlation for wild monkeys, even though grooming functions for more than just hygienic purposes. The present study also seems to support this assertion, in that autogrooming did not exceed allogrooming. Time spent autogrooming was relativity high while time spent allogrooming was relatively low in comparison to wild monkeys (see chapter 5 for allogrooming discussion). It is possible though that the high amount of autogrooming in captivity may be indicative of stress. However, given that social grooming was also decreased it seems likely that there is something in the captive environment which is decreasing the need for social affiliation, compelling monkeys to autogroom more often.

Results for male and female autogrooming behavior appears to correlate with the literature. Males have been reported to autogroom more than females (Kurland 1977).

Though the results of the captive study are not very different for males and females, males were found to autogroom slightly more than females. 55

CHAPTER 5. RESULTS AND DISCUSSION: SOCIAL BEHAVIORS

Social behaviors are important in understanding the overall health of the captive macaque population. These behaviors include allogrooming, play, sexual behavior and agonism. Though social behaviors (18%) were not observed to constitute as much of the activity budget as non-social behaviors (82%) they are certainly essential in that Japanese macaques, like most primates, are highly social creatures.

Allogroom

Allogrooming consisted of time engaged either removing objects from the hair of another monkey or receiving this service. All monkeys were observed to engage in this behavior. However, the male Nikko at Minnesota was never observed, either through focal or ad libitum observations, to direct grooming towards another. He only received allogrooming. Allogrooming behavior typically involved only two monkeys, though on a few occasions grooming parties of three individuals were observed. Attempts were made to link allogrooming behavior to kin groups.

100 - 90 80 70 ~ 60 - ~ 50 - 40 - p" 30 - 20 - 10- 0, 0~~ ~tifi ~~,~ ~~,~~ ~~,~ ~~~ ~o~o ~~~5 ~ ~ ~~~ ~ ~ ~ ,~o ~~ ti .~,~ ~ 4`a~~~~~ 5 ~ ~ti

Subject

Figure 5.1. Allogrooming at the Blank Park Zoo 56

100 - 90 - 80 - ~ 70 - ~ 60 - ~ 50 - ~ 40 - ~-' 30 - 20 -~ 10~ ~~ ~..~~ 0 \~ 7 •~~ ~~~~ ~~e~ ~~° ~~~ ~~~ ~~ ~Ss~ ~~~ ti~~~ ~" ~~ ~ ~~

Subject Figure 5.2. Allogrooming at the Minnesota Zoo

According to Figures 5.1 and 5.2, there is a considerable amount of allogrooming differences among monkeys in the study. As is shown in Table 5.1, at Blank Park the amount of time spent allogrooming was 19.1% (range 7.8% - 38%) of the time budget.

While at Minnesota this value was 16.0% (range 7.6 % - 31%). ANOVA tests did not reveal any significant differences between zoos (ANOVA: d.~1; p=0.327).

Table 5.1. Comparison of the time spent allogrooming by monkeys Subjects Percentage All Monkeys 17.8 Blank Park 19.1 Minnesota 16.0 All Males 15.9 All Females 18.2 Blank Park Females 20.2 Minnesota Females 15.9

Attempts were made to correlate allogrooming patterns with kin relations. Twenty- seven percent of the total allogrooming bouts at the Minnesota Zoo (N=139) were between kin members, while 73%were between members of different kin groups. At the Blank Park

Zoo, the statistics were similar, with 36% of the total allogrooming bouts (N=252) between 57

kin members and 64% between members of different kin groups. Agonistic encounters were occasionally reconciled through allogrooming. Table 5.2 shows the number of

reconciliations observed between monkeys after agonism.

Table 5.2. Reconciliation observed according to kin group affiliation Blank Park Zoo Minnesota Zoo Ian Subjects Number Subjects Kin Groups Number Groups PalelTres B!F 2 Heather/Stern Rheus A/ Rotte 1 Rheus B / Rheus 1 Ole/ Tinker C/C 1 Doris/Flo B Blue/Gizmo C/F 2 Lena/Limpy C/A 1 Norma/Shera C/E 1 Blue/ Tres C/F 1

Table 5.3 compares allogrooming between wild and captive Japanese macaques.

Allogrooming is a more prominent part of the activity budget for wild monkeys at

Yakushima than for the monkeys in captivity. Wild female Japanese macaques engage in allogrooming 34.6% of the time. Allogrooming in captivity for females was much less, with

20.2% at Blank Park and 15.9% at Minnesota. This trend was also observed between wild and captive males. Yakushima males spent 26% of their time allogrooming, compared to only 15.6% at Blank Park and 17.3% at Minnesota.

Table 5.3 Percentage of time budget spent allogrooming by captive and wild macaques Site Females Male (s) Yakushima 34.6% 26.0% Blank Park 20.2% 15.6% Minnesota 15.9% 17.3% Zoo Average 18.2% 15.9% 58

Discussion: Allogrooming

Grooming has multiple functions, being both hygienic and important in securing social bonds. Allogrooming in this study partially conforms to what is reported in the literature. It was expected that this behavior in captivity would be as important if not more important than in the wild, due to the need to reduce tensions within a closed environment.

However, a very large difference was found for allogrooming between wild and captive macaques, with captive macaques spending less time engaged in this behavior. This decrease in allogrooming, and in fact all social behaviors at both zoos may be aconflict-avoidance strategy. Aureli and de Waal (1997) describe chimpanzees in captivity that display reduced social behavior, including allogrooming and aggression. This strategy reduces the possibility of conflict. Though many other studies note aggression and allogrooming as increasing with captive macaques, Judge (2000) discusses how coping mechanisms to captivity may not be limited to species type. These mechanisms may vary with the specifics of the environment and with individual qualities.

This study correlates well with what is known of wild male Japanese macaque allogrooming, at least in .form, rather than quantity. Pavelka (1993) notes it is not atypical for males to allogroom considerably less than females. Though male allogrooming could not be thoroughly examined at Minnesota, grooming between Blank Park males did not account for a large percentage of the total number of grooming bouts. At Yakushima, Tsukahara

(1990) reported that grooming differed between males of different ranks. He observed that the alpha male never groomed other monkeys. This is similar to what was observed for

Nikko, who was never seen to groom others. However, Sam, the dominant male at Blank 59

Park, was observed to groom other monkeys, including those of low rank. Tsukahara (1990) also found that females groomed the alpha male but did not solicit grooming in return. This was also characteristic of the dominant males at each zoo in the study. Females did not appear to solicit either Nikko at Minnesota, or Sam at Blank Park to groom them. Tsukahara

(1990) hypothesized this to be due to female need of males for territorial defense. Though territorial defense is not a reasonable explanation for female grooming of the alpha male in zoos, it is reasonable that females would desire a close bond with the alpha male for coalition support.

Allogrooming between and within kin groups appears similar to what has been found in other studies. At the Arashiyama West troop, members of the same kin group were observed to groom one another 35.3 % of grooming interactions, with the remainder being between kin groups (Ando 1988). This is very similar to what was found at both zoos.

Within kin group allogrooming consisting of 27% at Minnesota and 36% at Blank Park of the total grooming bouts. These values between wild and captive macaques are similar despite the often much larger size of the kin groups in wild or free-ranging situations where reproduction is not restricted. On Koshima Island, Kurland (1977) reported that kin groups consisted of five —eighteen individuals. This is much different from captivity, with two - three members in kin groups at Minnesota and two -seven members in groups at Blank Park.

However, the percentage of the population who are kin is similar, with 8-25% of the wild population being of the same kin group and 10-20% of the captive groups being kin. What is dissimilar between wild and captive kin groups though is the composition of the kin groups in terms of mothers and daughters. Most wild females of reproductive age have daughters to socially groom with, accounting for 70% of total grooming among females (Ando 1988). 60

The lack of offspring for many females in the zoo inevitably changes this species-specific behavior.

This study also supports recent additions to the literature in regards to the behavior of older females. Pavelka (1991) discussed the sociability of old female Japanese monkeys in response to claims by Nakamichi (1984) and Hauser and Tyrell (1984) that activity and social engagement decreases with age. In her study of free-ranging Japanese macaques in

Texas, she found no evidence that older females spend less time engaged in social interaction

(Pavelka 1991). In fact, sociability is linked to kin ties. In some occasions it may appear that older females are less social, but this is only if they are left in a group without any female kin

(Pavelka 1993). Female kin ties are extremely important in Japanese macaque society.

Pavelka (1993) notes that kin are the core of social interactions. In her study she describes one old female, Ranny, who did not have any female kin as a "loner" (Pavelka 1993:28).

Absence of female kin resulted in a lack of social grooming partners for Ranny. It also meant that she had no support from others in conflicts, hence she was a very low ranking female. The only female in the study without any known kin is Big Belly at Blank Park.

Contrary to Ranny though, Big Belly was often observed in social interactions; however, it is likely she is a low ranked member of the troop. As kin groups were not the major source of grooming for monkeys at either zoo, this result is not unexpected.

Reconciliation was a rather rare event at either zoo. This is to be expected though since it only occurred after an agonistic encounter. Blank Park monkeys were observed to reconcile more often than Minnesota monkeys, with eight reconciliations at Blank Park and only two at Minnesota. Schino et al. (1998) found that reconciliatory events were less frequent during the mating season. They noted that kin were more likely to reconcile than 61 non-kin, but in general these macaques are very flexible in their conciliatory tendencies.

Observations of wild macaques do not correspond to the results from this study, in that only one of the ten reconciliatory events were between kin. Kutsukake and Castles (2001) discuss the "integrated hypothesis" of reconciliation in Japanese macaques. This hypothesis predicted reconciliation based on high levels of stress due to aggressive encounters between individuals who possess a valuable relationship (Kutsukake and Castles 2001). In their study of wild provisioned macaques in Japan they found that reconciliation occurred after one of seven aggressive encounters. This proportion was not found for captive animals.

Additionally, Kutsukake and Castles (2001) observed that self-directed behaviors, scratching, and self-grooming, were likely after an aggressive event, and were more frequent when that aggressive event was with kin, but decreased after reconciliation. The authors believe this finding supports the notion that reconciliation decreases stress between animals and that the most stress is induced by agonism between kin members (Kutsukake and Castles 2001).

This study did not clarify the debate as to the structure of grooming in Japanese macaques. Seyfarth's (1977) model, which predicts female competition to groom the highest ranked females, thus resulting in grooming pairs of adjacently ranked females, is not supported by this study, in that monkeys of very different ranks were observed to allogroom.

Seyfarth (1977) links this desire to groom with the highest ranked individual to coalition support. It is possible that the lack of competition for food has resulted in a lack of a need for coalitions, thus lessening the need to ally with only the highest members of the troop.

Coalitions were only possibly observed for a few individuals in the study. One coalition, between Fro and Pippin, the alpha female and the most subordinate male, in particular does not give support to the hypothesis that coalitions would exist only between adjacently ranked 62 individuals. It should be noted that it is very possible (and likely) that more coalitions exist, but were not recognized over a short study period (see section on agonism for further discussion on coalitions).

Play

Play is defined as an affiliative interaction between at least two individuals, consisting of jostling, pulling and jumping on one another. Play was only observed between certain monkeys at Blank Park. Often this behavior would begin between a pair of monkeys, and others would join in. Figure 5.3 displays the number of observations recorded of this

10-

~ g-

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0~ O Gizmo Lena Merry Ole Pale Pippin Shera Tinker Tres

Subject Figure 5.3. Play behavior observed at the Blank Park Zoo behavior either through focal or ad libitum observations. Cleary, Pippin was most likely to engage in play with the others (N=11). This behavior was not observed, either through focal or ad libitum observations, at Minnesota. The data for this category were not normal and so

ANOVA tests were not conducted. As Table S .4 shows, the percentage of time spent engaged in play by monkeys was very low. Only 0.12% of the budget was spent in play 63 when all monkeys at Blank Park were considered. Males, though, were found to be more likely to play than females (0.36% and 0.02%, respectively).

Table 5.4. Time spent in play by monkeys at the Blank Park Zoo Subjects Percentage All Monkeys 0.12 Males 0.36 Females 0.02

Discussion: Play

Play was not a common occurrence for captive Japanese macaques in this study. A study by Pellis and Iwaniuk (2000) concurs with this observation, noting that for wild Old

World monkeys play is a relativity rare behavior among adults. They note however that adult play does have a functional significance. Brueggeman (1978) hypothesized in his study of rhesus macaques (M. mulatta) that play is often used for social assessment. Pellis and

Iwaniuk (2000) tested this hypothesis by examining a wide range of primate taxa, including

Japanese macaques and found support for Bruggeman's (1978) hypothesis. They concur that the function of play is mainly for social evaluation and manipulation (Pellis and Iwaniuk

2000). Many other functions of play have been hypothesized and include social communication and integration, and maintenance of the dominance hierarchy (Smith 1978).

It is possible that the monkeys at Blank Park were, as Bruggeman (1978) suggests, evaluating their social situation in the troop, or it is possible that the play behavior may be related to one of the other reasons for play.

Play was not observed at Minnesota, probably due to the lack of multiple males. At

Blank Park, the males were almost always the initiators and main participants of play. This concurs with the literature, which reports a higher incidence of play among adult males than females (Penis and Iwaniuk 2000). 64

Sexual Activity

Sexual activity was a rare event at both zoos. Only five monkeys were observed to engage in this activity (Nikko, Anna and Boo at Minnesota; Sam and Pale at Blank Park).

Only 0.16% of focal observations at Minnesota were of sexual behavior. This figure is similar at Blank Park, with only 0.11% of focal observations of this behavior. This low frequency is expected since data were collected during the non-breeding season. Series mounting behavior though was observed on two occasions between Nikko and females, Anna and Boo, at Minnesota. This was clearly not behavior related to dominance, judging by the relative separation of the pair from the other monkeys, multiple mounts, and general affiliative behavior between the pair. Also, during the Nikko/Boo mounting breaks, it appeared as though Boo was anxious with Nikko's spacing between mounts. She was observed to nervously glance in his direction, and even once tried to mount him. This mounting behavior can best be described as a series mount, which is indicative of the

Japanese macaque mating style during the breeding season. On both occasions a series of mounts (seven mounts total for each pair) were performed. Though this did appear to be a series mount, ejaculation was not observed. Instead, the mounting sequence simply ended with one monkey beginning to engage in another activity, such as foraging.

The sexual category also includes self-manipulation of the genitals, which was only observed during focal periods for Pale and Sam, both males at Blank Park. Focal observations showed Pale spending approximately five minutes of the total four hours of observations engaged in this behavior. Sam spent only 25 seconds in this behavior. These monkeys were also observed to engage in genital self-manipulation during ad libitum observations, but it was not considered to be a regular activity. This behavior was also noted 65 during two ad libitum observations of Nikko at Minnesota. As with males at Blank Park,

Nikko did not often engage in this behavior.

Discussion: Sexual Behavior

Sexual behavior only constituted a very small proportion of time for the captive animals in this study. This is not surprising given that data were collected during the non- mating season. The copulatory acts between Nikko and Anna, and Nikko and Boo, are therefore uncharacteristic. All of the observations indicate behavior characteristic of a copulatory event: multiple mounts spread over a long period of time and close contact to one other between mounts (Pavelka 1993). However, Japanese macaques are not normally expected to copulate during the non-mating season. However, females who fail to conceive during the breeding season will continue to come into estrus throughout the year (Chopra et al. 1992). Chopra et al. (1992) explain that males become sexually active during the non-

breeding season due to olfaction commutation, smelling hormonal changes in females.

Therefore, even though this behavior was not expected, it is not inexplicable.

Female —female homosexual behavior was not observed as it has been in the wild although it might be expected in captivity. Wolfe (1984) describes the mounting behavior

between females as occurring during the breeding season when male variability is lacking.

At Arashiyama West, she hypothesized that the skewed sex ratio and the lack of novel males resulted in an increase in this behavior. Future research into the Japanese macaques in this study may address whether or not homosexual activity is present for females in zoos during the breeding season, since they too have a limited and non-novel set of males.

The occurrence of masturbation was a rare event at the zoo. Erwin and Deni (1979) note that in some captive cases masturbation is a frequent and stereotypic behavior. Due to 66 the low frequency of this behavior it is concluded that macaques at both zoos are not engaging in this behavior any more than their wild conspecifics. Only males were observed to engage in this behavior, though both males and females have been observed to engage in this behavior in the wild and in free-ranging situations (Wolfe 1984; Domingo-Roura et al.

2004). Wolfe (1984) observed 27 incidents of masturbation in her study of the females of

Arashiyama West. This behavior was not limited to the breeding season, or to females in estrus. Wolfe (1984) noted that this behavior was found to be more prevalent in females belonging to two of the matrilines in her study; suggesting to her that this may be a learned behavior. Since this behavior was never observed of females at either zoo, it is possible that females simply have not learned this behavior.

Agonism

Agonistic activities included face threats, lunges, chases, physical attacks, displays, displacements, and mounting (non-sexual) behavior. Typically, when aggression occurred between monkeys, it usually consisted of a face threat and possibly a lunge. Only on one occasion, at Blank Park was a physical attack observed, where the monkey was actually wounded by another. Observations of recent wounds on monkeys were noted on several more instances during the study period, though the attack itself was not observed. Agonistic behavior was used to construct the dominance hierarchy. As Figure 5.4 and 5.5 show, agonistic activities did not comprise as much of the activity budget as other behaviors. Some monkeys were never observed, through focal observations, to engage in this behavior. Ad libitum observations however revealed that all monkeys at both zoos were engaged in some type of agonistic behavior during the study. 67

1.4

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Figure 5.5. Agonistic activities at the Minnesota Zoo

These observations also accounted for a very small amount of the time budget, though attempts were not made to record duration of any ad libitum observations. As Table 5.5 illustrates, Blank Park monkeys spent 0.4% of their time in agonistic behavior (range 0% —

1.3%). The Minnesota monkeys exhibited a slightly higher amount of agonism, spending 68

0.5% of their total time budget engaged in this behavior (range 0% to 1.2%). Despite the finding that agonism was not a very prominent part of the monkeys' activity budget, analyses did reveal that data were considered normal and hence ANOVA analysis was conducted.

The ANOVA test was conducted for focal sample data, which did not include displacements

(only recorded ad libitum). ANOVA analysis did not reveal a significant difference for this activity between zoos (ANOVA: df 1; p=0.374).

Table 5.5. Comparison of time spent in agonistic behaviors Subjects Percentage All Monkeys 0.4 Blank Park 0.4 Minnesota 0.5 All Males 0.5 All Females 0.4 Blank Park Females 0.3 Minnesota Females 0.5

Blank Park Zoo

Zoo

2 n n n r~ Bilbo Fro Pale Pippin Sam Tres Boo Heather Liza Nikki Subject Figure 5.6. Displays observed at both zoos

Displays were only noted for ten monkeys throughout the study. Display behavior typically involved shaking a tree that the monkey was in, or in the case of Blank Park, climbing the wire cage and shaking the walls of the exhibit. This behavior was observed when other macaques were with the displaying individual in the same tree, in which case the 69 other monkeys simply held onto the tree until the display had stopped. Animals were not often observed to actually leave the tree following or during displays. Figure 5.6 illustrates the amount of displays observed at either Blank Park or Minnesota through both focal and ad libitum observations. Among monkeys at Blank Park, males were more likely to display than females. Pippin was observed to display five times, followed by Pale and Bilbo who each displayed three times. The dominant male, Sam was not observed to display throughout the study. All females who were observed to display at either zoo were relatively high ranking.

Dominance mounts were observed at both zoos, though only once at Minnesota.

Dominance mounts consisted of a single mount between monkeys. On one occasion a mount was observed involving three monkeys at Blank Park; however, this observation was made early in the study and the identities of all the monkeys were unknown. The mount involved two females, one of which was Smee and one unknown male. Table 5.6 describes mounts at each zoo, recorded through focal and ad libitum observations, in which the mounter and the mountee were identifiable.

Table 5.6. Dominance mounts observed during study Zoo Mounter Mountee Number Blank Park Limpy Merry 1 Merry Bilbo 2 Merry Lena 2 Merry Pippin 1 Pale Merry 1 Pale Tres 2 Pippin Gizmo 1 Pippin Pale 5 Pippin Sam 2 Pippin Shera 1 Sam Merry 1 Sam Bilbo 1 Minnesota Susie Margie 1 ~o

The most significant number of mounts was seen for Pippin who mounted Pale five times, and also mounted Sam, the dominant male, twice. One of the observations occurred immediately after Sam had directed aggression towards Pippin. In both instances where

Pippin mounted Sam, Sam pushed him off, but the situation did not escalate into further agonism.

Aggressive interactions, involving face threats, chases, lunges, attacks and displacements were used to construct the dominance matrices (Tables 5.7-5.9). The female and male dominance matrices (Table 5.8 and 5.9 respectively) at Blank Park were not integrated, owing to the fact that agonistic encounters were not observed between all males and all females. These observations were collected both through focal and ad libitum observations. Heather, the dominant female at Minnesota, was observed to be the dominant individual involved in the most agonistic occurrences (N=45). At Blank Park the most agonistic interactions were observed for Lena and Limpy (N-17 and N=20, respectively). In sum there were 135 agonistic encounters for monkeys at Minnesota, averaging to a rate of

0.44 interactions per hour of study. At Blank Park, 152 agonistic interactions were observed, which averages to approximately 0.5 5 interactions per hour. Only eleven of the Blank Park aggressive attacks observed involved males. The remainder of the aggressive encounters

(N==106) were between females. One case of redirection of aggression was observed at Blank

Park. In this instance Fro attacked Tres, who then attacked April, who had been nearby.

Several possible coalitions were also observed at Blank Park. The clearest evidence for a coalition was observed between Pippin and Fro. On three occasions, Fro supported Pippin.

In one case, Toto screamed at Pippin, who withdrew as Fro chased Toto. In two other 71

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Table Q H 73 instances, Pippin was threatened by Limpy. Pippin retreated to Fro and proceeded to follow her wherever she went in the compound. During this time he appeared to be nervous, glancing often in Limpy's direction. Other possible coalitions involved Fro/April,

~le/Binky, and Big Belly/Limpy. These consisted of single observations though and are not considered as solid evidence of any long lasting coalition.

It appears that there is a hierarchy of kin groups among the macaques studied, especially at Blank Park. The order of most dominant to least at Blank Park being: group A,

B or F, C, and E. Big Belly (group D) is either above kin group C or E. At Minnesota, the hierarchy of matrilines is not as clear, with Rheus A and Rotte members typically being dominant, and Nose and Rheus B typically subordinate (Betts members are somewhere in the middle).

Discussion: Agonism

Agonism made up a small part of the activity budget for the monkeys in the study.

Both zoos are rather similar to one another, with agonism making up less than one percent of the total time budget at each zoo. However, when the data were scrutinized more closely it was found that a number of these occurrences were greater at Blank Park for some types of agonism, and greater for others at Minnesota. In particular, displays and dominance mounts were more frequent at Blank Park. Since most of these behaviors involved males, it is not surprising that Blank Park would have a higher occurrence of these activities. At Blank Park,

Pippin was frequently observed in agonistic situations —often displaying or mounting other males. His mounting of the alpha male Sam, and several of the other males suggests that he is struggling to gain a higher rank. However, Pruetz (1999) notes that mounting is considered a low intensity form of agonism in that it does not involve access to resources 74 typically characteristic of other types of agonism such as displacements. Hence, in these situations, Pippin's mounting of other males is not interpreted as being as important as other forms of agonism (e.g., displacements, chases) in determining dominance, in which case the other males were always dominant to Pippin.

It was observed that the Japanese macaques in captivity express a pattern of a stable, linear dominance hierarchy as is expected from comparison to wild macaques (Pavelka

1993). This linear hierarchy is especially seen at Minnesota, where very few rank reversals

(in which a normally subordinate animal supplants a dominant individual) were observed.

Nearly 2.9% of agonistic encounters at Minnesota exhibited reversals (Table 5.7). No rank reversals were observed for males at Blank Park (Table 5.9). The hierarchy of Blank Park females expressed many rank reversals (13.2% of all encounters) indicating that at Blank

Park the female dominance hierarchy is not as linear as one would expect for this species

(Tables 5.8). Hill and Okayasu (1995) note that rank reversals are expected in 3.5% of agonistic encounters. However, at Blank Park, the number of reversals is much higher than a linear hierarchy would predict, indicating that something is affecting the normally species- specific linear dominance hierarchy.

In the wild, kin are essential for support and maintenance of this hierarchy (Watanabe

2001). One of the main questions addressed in the study regarding dominance is how dominance is determined and maintained in the captive setting. Since kin are essential for maintenance of the female hierarchy, it seemed likely that those females without large kin groups would be rather low ranking. They lack the support necessary to contest other monkeys. Based on this, one may expect that the larger the kin group in the zoo, the more likely the individuals within that matriline are dominant to others. This is clearly not true at 75

Blank Park where the size of the matrilines was fairly variable. Group C, which includes

Baldy and her progeny, was not a particularly high ranked kin group despite the fact that this matriline was nearly double the size of many of the other families, including the dominant kin group A. Also, at Blank Park, Big Belly, the only female without any known kin is rather low ranking. This correlates well with Pavelka's (1993) observation that low ranking females often do not have well defined kin groups. However, observations of Big Belly's interactions did not reveal that she is the lowest ranked individual in the group.

When constructing the dominance hierarchy it was observed that the youngest sibling or the mother was not always the dominant individual in an agonistic encounter. The rank of siblings in Japanese macaques is expected to follow the "youngest ascendancy" model with the youngest sibling holding the highest position of rank below the mother (Kawamura

195 8). Pavelka (1993) supports this model, in that mothers were always observed to be dominant over daughters in her study of the Arashiyama West monkeys. She also observed that among sisters, the youngest was dominant. However, despite support for the model, Hill and Okayasu (1995) noted that dominance relations in females do not always follow the

"youngest ascendancy" pattern. In a study ofnon-provisioned macaques at Yakushima, elder sisters were always observed to be dominant over the younger sister. Hill and Okayasu

(1995) link this pattern to the lack of support from the mother (mother was not observed to aid daughters). They predicted that the youngest ascendancy pattern is likely when provisioned resources concentrate feeding in a particular location resulting in frequent aggression (Hill and Okayasu 1995). Studies have shown that the support of the mother for the daughter is key in ascending the dominance hierarchy (Datta 1983). These findings concur well with observations made at both zoos. In many cases the youngest sister was 76

dominant over her siblings, but in others this was not the case. Mothers were either absent or

for some reason not giving their daughters support in encounters.

For wild monkeys agonism is also not a dominant part of the time budget, though it is

noticeably more frequent than for monkeys in this study. Hill and Okayasu (1995) reported

1.40 agonistic events per hour in their study of the Yakushima macaques. This is much higher than the 0.44 (Minnesota) and 0.55 (Blank Park) interactions per hour observed during this study. This may be further support for the hypothesis that these macaques are using some type ofconflict-avoidance strategy (Aureli and de Waal 1997). Aureli and de Waal noted that both aggression and affiliation have been found to decrease in captive chimpanzees. In comparison though to provisioned situations, which have been found to increase aggression by thirty times the natural rate, both Yakushima and captive macaques do not display much agonism (Mori 1977). Provisioning creates tensions by congregating individuals around key resources. Monkeys in this study appear to be more similar to unprovisioned monkeys in the amount of agonism displayed despite their similarity to provisioned monkeys in that their food is congregated and provided for them. However, as observations of indoor feeding were not available it is quite possible that agonism is actually much greater in the captive troops, and more similar to the provisioned monkeys. ~~

CI~[APTER 6. S Y A►ND CONCLUSIONS

This study has sought to address whether the species-specific behaviors of Japanese macaques are being displayed in the zoo setting and what factors may be affecting these behaviors. It was not expected that the captive macaques would display the behaviors at the same frequencies as seen in the wild. Melfi and Feistner (2002) note that even expecting similar activity budgets for wild animals is problematic due to the variation in environments.

However, some behaviors that were observed in captivity, in particular, periods of inactivity, foraging and grooming, are considerably different from the behavior of wild macaques.

Summary

Monkeys at both zoos studied can be characterized as being very inactive, with inactivity levels of 46% at Blank Park and 39% at Minnesota. The differences in the environments of the respective zoos does not seem to affect time spent inactive. The question is whether this much time spent inactive can be considered aberrant behavior. The inactivity level seen in captivity is certainly much greater than that in the wild, as least for females. This is evidence that this species-specific behavior is not being expressed at the same frequency in captivity as in the wild.

Feeding behavior varied significantly by zoo, with Minnesota females and all males feeding at similar frequencies to their wild counterparts. However, at Blank Park, females spent an extraordinarily low amount of time feeding (10.6% of their time). It is possible that the Minnesota macaques forage more because they actually have to search for their food.

The monkey biscuits at Minnesota are only available in the indoor enclosure. This entices the monkeys to search for the scattered peas and hidden food items in a way that is more 78

similar to wild macaques. At Blank Park, the monkey biscuits are readily available during the day; thus, when monkeys are hungry they are not encouraged to search for food.

At both zoos, the diet is certainly not as stimulating or as varied as it would be in the wild. Wild Japanese macaques are generalists, eating fruits, leaves, insects, and some meat

(Hill 1974). Procurement of these foods would not only entice monkeys into exercise, but would also provide a stimulating diet. Following the species-specific dietary repertoire of the animals is important for both enhancing nutrition and exercise (Pruetz and McGrew 2001).

And since enhancing foraging is an effective type of environmental enrichment, it would increase the mental stimulation of the animals as well.

In the wild many primates often spend most of their day foraging. The high amount of inactivity in captivity is usually the result of the lack of foraging opportunities for the animals (Maple and Finlay 1989). This lack of foraging may explain the inactivity of Blank

Park monkeys, but it does not explain the behavior of Minnesota females, who foraged more but still had high inactivity levels. It may be that other factors of the captive environment are more important in inducing inactivity as well. Females in the wild have infants to care for, food to find, and large extended kin relations to maintain. The lack of infants in the zoo setting may be unhealthy for females, in that females are expected to socially groom most with their offspring (Ando 1988). Minnesota is attempting to remedy this situation with their captive troop; however, at Blank Park, breeding of the animals is not planned.

Obesity is a problem for several of the individuals at both zoos. This is probably due to a lack of exercise (Bennett and Davis 1989). Individual metabolism though must play a role into obesity, as it does with humans, since not all extremely inactive monkeys were obese. To reduce obesity in some of these monkeys, it may be necessary to simply find out 79 what type of feeding enrichment would increase activity levels. Primates in captivity are often very willing to work for their food (Markowitz 1979). The goal of both zoos should be to determine what type of foraging work would most interest some of these obese monkeys, engaging them in some type of activity. Obesity at both zoos may also be affected by the public's interest in feeding the animals. As Croke (1997) noted, public feeding of animals often makes it impossible to control diet. This problem of visitor feeding, however, was not observed at Blank Park, where they also have obese animals.

Related to time spent inactive and foraging is time spent moving. Wild macaques spend nearly twice the amount of time moving as captive macaques. Just as captive monkeys have no infants to tend to, they also have relatively nowhere to go. This is probably an area of the species-specific repertoire that is unavoidably different between captive and wild populations. Even at Minnesota, where the animals had a much larger cage, monkeys were not observed to move significantly more. Unless the captive troops are exhibited in a very large enclosure, with opportunities for the entire troop to move to different areas, there is no way to really increase time spent moving in this way.

Adding complexity to the environment has been found to increase moving time and foraging, and decrease inactivity. Swaisgood et al. (2003) maintains that enclosures need to be complex (regarding topography, vegetation, and space), rather than simply appearing natural, to be stimulating to the animals. Both zoos studied can be characterized under

Maple and Finlay's (1989) "soft" zoo environments, in that they appear natural. It is possible though that that this "soft" environment is not actually complex enough to entice monkeys to be active, especially through foraging and moving. The complexity of the environment is apparently not as stimulating to the macaques as the wild environment, since they spend so 80 much time inactive, and less time foraging and moving throughout their enclosure. The two zoos differ regarding environmental complexity, with more vertical climbing opportunities within the Blank Park enclosure, and a larger terrestrial space at Minnesota. It seems likely that these more varied methods of moving are stimulating the Blank Park animals, especially given that they have less terrestrial space available. It is possible that factors other than enclosure size are crucial to affecting moving, foraging and inactivity time. Despite the smaller cage at Blank Park, monkeys were not observed to differ significantly in time spent moving from Minnesota macaques. It is possible, though, that the smaller enclosure is related to the decrease in foraging at Blank Park, in that individuals have less space to search for food.

Adding complexity to the environment may also serve to increase time spent manipulating objects, particularly in more positive ways than what is currently seen. Object manipulation at both zoos often involved behavior that may not be beneficial to the health of the monkeys. At Minnesota, object manipulation most often involved biting/playing with objects that zoo visitors had dropped into their cage. However, due to primates' susceptibility to disease and that object manipulation often led to ingestion, whether the item was edible or not, it may be beneficial for the zoo to provide other opportunities for the monkeys to manipulate objects. Perhaps the addition of toys, puzzle feeders or other safe objects would be appropriate. This observation can also be made at Blank Park, where object manipulation involved picking the paint off of the cage walls, sometimes leading to ingestion. Some monkeys of the troop seemed to benefit from enrichment items (e.g., balls, birds). Perhaps the addition of more enrichment items, so that more than just high-ranking 81 individuals can use the items, and adding them more frequently to the exhibit would be beneficial.

Grooming behavior of captive monkeys, both social and nonsocial appears to be the opposite of what is characteristic for wild Japanese macaques. Wild monkeys spent much more time engaged in social grooming, and much less time autogrooming than captive conspecifics. This seems to suggest that maintenance of social bonds is not as important to captive macaques. This is an unexpected finding considering many studies have pointed to the importance of social grooming in primates. The need to maintain social harmony within the group through grooming was originally hypothesized to be very important, in that zoo animals do not have the ability to escape from one another; thus, it is vital to maintain good relations. It was also expected that reconciliation would be important in repairing damage to social bonds (Stammback and Krummer 1982; Kutsukake and Castles 2001). However, very few observations of reconciliation were observed after agonistic encounters, thus supporting the conclusion that perhaps the maintenance of social bonds within the captive situation is less important than in the wild.

The importance of kin ties appears similar in the captive situations as in the wild, despite social relations in general being altered. In the wild, matrilineal kin are the most important social network (Pavelka 1993). Many grooming occurrences did occur within kin groups, even though more grooming was observed between groups. This is not unlike what has been seen in the wild (Ando 1988). The size of the kin groups was very small in this study, with some matrilines only containing two members. It is possible that kin relations are reduced though in that some kin groups were never observed to groom within their group, grooming outside of the kin group instead. If kin relations were as important as in the wild, 82 one would expect that kin would groom at least to some extent. Kin relations have likely been effected by captivity, though precisely how is not perfectly evident.

Since social grooming in general was much less frequent in captive macaques than in the wild, perhaps social bonds are simply not as important to captive macaques. The lack of feeding competition in the zoo may be related to the decrease in social affiliation. Monkeys in the zoo may not need to create the same extended alliances as in the wild. In the wild these alliances are often linked to accessing resources, which in the zoo will be readily available to all individuals. The lack of competition for resources within zoos may reduce the need to cultivate social bonds to create alliances to the same extent as in the wild.

Additionally, the troops may be practicing some type of conflict-avoidance strategy, which would result in a decrease in affiliative and agonistic behaviors (Aureli and de Waal 1997).

The skewed sex ratio at both zoos has the possibility of being detrimental to two social activities in particular: play and sexual activity. Though it is not clear in the literature what a "normal" sex ratio is, a skewed sex ratio can impact the population (Furuya 1957;

Maruhashi 1981; Sugiyama 1976; Wolfe 1979). Female homosexuality is linked to the presence of a skewed sex ratio (Wolfe 1979). However, no homosexual encounters were observed during the study. Additionally, an extended discussion on sexual activity is not warranted in this present study since data were collected during the non-breeding season.

There were very few instances of this behavior recorded and what was observed was not abnormal. The sexual behavior observed did appear to be species-specific, though a detailed study during the mating season is necessary to confirm this.

The observations on play behavior seemed to indicate a healthier state at Blank Park.

At Blank Park, multiple monkeys engaged in affiliation with one another through play. This 83 behavior is linked to social evaluation and manipulation (Bruggeman 1978). These social engagements allowed monkeys to actively interact with others in a varied way, depending on the participants and the type of play. In general, it seems possible that individuals who engaged in play were more stimulated in their environment than those who did not play.

Since play behavior is observed in Japanese macaques in the wild, it would be expected to see this behavior in captivity (Pellis and Iwaniuk 2000). Affiliative behaviors were limited to social grooming at Minnesota. Since adult play is more prominent in males, it is likely that the lack of multiple males is the reason play was not observed at Minnesota. Hopefully, the addition of males to the zoo will increase the likelihood of this behavior; indecently, a new

male was added Fall, 2003.

Play behavior is also related to dominance and agonism, in that it may function in

monkeys' evaluation of their social situation within the troop (Bruggeman 1978). Though analyses did not reveal any significant differences between zoos in terms of agonism, the zoos differed in terms of the types of agonism exhibited. At Blank Park, more mounts and displays were observed. This can be explained by the presence of males, though females also participated in these behaviors occasionally. These behaviors were rare at Minnesota. This difference may indicate that individuals at Blank Park, in particular males, were actively engaged in maintaining their position in the dominance hierarchy. The several mounts of

Sam by Pippin indicate that Pippin may be trying to ascend the hierarchy, though all other signs point to Sam's dominance to Pippin, and all other males. Minnesota monkeys were often observed in aggressive chases and displacement behaviors. There were no obvious signs that any individual was trying to change her position within the hierarchy, supporting the stable, linear dominance hierarchy characteristic of the species. Observations of social 84 evaluation and manipulation, through mounting, displaying, displacing and playing, all indicate that captive monkeys are interested in their social relations and their place within the troop. Their placement in captivity has not deprived them of this species-specific behavior.

The low occurrence of wounding suggests that agonism, though present, does not often escalate into violent attacks at either zoo.

Despite the likelihood of stereotypical behaviors occurring within the zoo setting, this was not observed for any animals. Neither qualitative nor stereotypical abnormalities were observed during the study. The presence of abnormal behaviors is the clearest evidence of an unhealthy mental state for an animal (Erwin and Deni 1979). Hence this lack of abnormal behaviors indicates that welfare at both zoos is relatively good. There is one possible aberration observed during the study. The high amount of inactivity at both zoos may be extreme enough to be considered abnormal. Abnormal behaviors are thought to be induced by many factors inherent of the zoo setting. In particular, despite the possibility that zoo animals can be adversely affected by visitor noise and the inability to escape from conspecifics, this was not observed. It is probably beneficial that both zoos allowed monkeys to at least partially hide from visitors and other animals.

Recommendations

Though all of the expected species-specific behaviors of Japanese macaques were observed in the captive setting at both zoos, the frequency of many of the behaviors was not similar to what is observed in the wild. Therefore, it would be beneficial to both zoo populations if some changes were made in the management of the animals.

Both zoos would benefit from the addition of infants and juveniles. Females are in particular very inactive. Since for females, time spent foraging at Minnesota was similar to SS what is seen in the wild, factors other than foraging must be responsible for the extended lnactivlty. The addition of infants would stimulate not only their mothers, but also many of the other group members as well. Minnesota is attempting to remedy this problem with their captive troop, by adding breeding males to the troop. However, at Blank Park, breeding of the animals is not planned. Perhaps additional enrichment devices could be added to the exhibit to try to engage the females in activity. Monkeys at Minnesota would benefit from enrichment devices as well, even if infants are eventually born. The addition of members into the matrilines may also help to create social bonds that are more similar to that seen in the wild.

Feeding activity needs to be enhanced at Blank Park. The low amount of foraging activity indicates that the monkeys are not actively looking for their food. Perhaps a program similar to that seen at Minnesota should be implemented. At Minnesota, the monkey biscuits are only available in the indoor enclosure. This entices the monkeys to search for the scattered peas and hidden food items in the outdoor enclosure in a way that is more similar to wild macaques. In addition to this strategy, puzzle feeders, or natural feeding methods such as whole fruits and difficult to process foods could be added to the exhibit (Reinhardt and

Roberts 1997). Reinhardt (1993b) suggests an enrichment strategy for monkeys housed in cages which may be suitable for Blank Park. In this enrichment strategy, the food items are placed above the cage ceiling, so that monkeys have to climb up the cage, and manipulate their hands through the cage to get the items. These strategies may entice monkeys to actively search for food. Additionally, this may be an effective way of trying to encourage activity in some of the obese monkeys in the study. 86

The addition of environmental enrichment items would benefit monkeys at both zoos.

As was seen at Blank Park though, only adding a few items to the exhibit (e.g., plastic balls) will probably only engage the higher ranked animals. It may be beneficial to try to add more items so that more monkeys may have the opportunities to use the items. Many recommendations of environmental enrichment involve adding something unnatural to the exhibit. Plastic toys, balls and puzzle feeders, it can be argued, take away from the natural set-up of the enclosure for the zoo visitors. These enrichment strategies may be very beneficial since the most important goal is to engage the animal in a way that it functionally similar to in the wild (Swaisgood et al. 2003). However, there also is evidence that using naturalistic items may be more beneficial to the animals than artificial items (Reinhardt and

Roberts 1997). Hence, enriching the animals with naturalistic items, such as scattered seeds and whole fruits may be an excellent way to enhance species-specific behaviors in the animals and also create a visually pleasing exhibit for the zoo visitors.

Significance of Study

This research has sought to determine if the captive populations studied are displaying species-specific behaviors in order to help solve captive management problems and provide the best possible environment for the animals. Applied primatology is the use of behavioral knowledge of a species to try to make the captive environment as natural and stimulating to animals as possible, reducing abnormal behaviors and promoting species- typical behavior (Maple and Finlay 1989).

This study is an anthropological investigation into the behavior of a fellow member of the order Primates. To biological anthropologists, preserving the species-specific behavior of fellow primates is crucial if we want to continue to study the species to reveal insights into 87 our own. Japanese macaques are a species that possesses culture, something we once thought was the defining trait of humanity (Shimahara 1970). These primates are also one of the few monkey species in which cultural transmission has been observed (Hirata 2001). Though the transmission of culture was not observed during this study, it could be observed at Minnesota if the animals begin to successfully breed. The macaques at Minnesota may in fact already have a cultural tradition in place. During observations it was noted that many macaques are missing hair, in particular on the backs of their head and neck. Conversations with the keeper indicate it is the mothers that are responsible for initiating this hair removal. Mothers have been observed to remove this hair when their infants are young and continue to remove it as they age. According to Minnesota keepers, the adults maintain their "hairdos" throughout life, either through auto or allogrooming. It is very possible that this is a culture of transmitting an "abnormal" behavior, as hair removal in the quantities seen here is not observed in the wild. If the Minnesota macaques are able to reproduce as the zoo hopes, this presents a fascinating future study for anthropologists interested in the study of culture in non-human primates, even if it is an "abnormal" cultural tradition.

Anthropologists, especially, should be interested in people at the zoo, since as

Hediger (1969) notes, people and animals are intrinsically linked in zoos. Observations of zoo visitors, though not systematically recorded in this study, support his discussion, revealing that zoo animals are having an effect on zoo patrons. While conducting observations, statements such as "they look so bored" or "why aren't they doing anything?" were often overheard. A systemic study of the reactions of zoo visitors would be beneficial.

These observations were noted despite the naturalness of the enclosure, which Maple and

Finlay (1986) related to visitors perceptions of animals as satisfied with their environment. 88

Additionally, Croke (1997) described zoo visitors speaking quietly and respectfully near naturalistic exhibits. However, despite the fact that both zoos were naturalistic, observations during the study period did not support these expectations. The opposite was often observed, especially at Minnesota, where visitors (mostly children) were often observed yelling and screaming at the monkeys. Perhaps this is simply the nature of children at the zoo, or maybe the enclosure type had some effect on the behavior of the visitors. At Blank Park, visitors see the monkeys up close (approximately one meter), while at Minnesota the monkeys are far below the visitors (approximately four meters). It seems possible that the distance between the monkeys and the visitors is creating a less personable experience at Minnesota, and perhaps creates less respect for the monkeys. As intrusive as the noise seemed though, there did not appear to be any negative effects on the behavior of the monkeys as some studies would suggest (Croke 1997).

Despite efforts made by both zoos, it did not appear as though visitors were really absorbing much knowledge about the animals. Most visitors merely walked by the exhibit, looked at the animals briefly than continued on with their tour. If one of the main missions of the zoo is to educate the public, than it would be hoped that zoo visitors would leave the zoo with some understanding of the animals that they saw. Both zoos do display information about the species. At Blank Park, the species name, range, diet and some behaviors are explained on a small display. At Minnesota, the educational materials are located indoors and explain not only the species range and food types, but also detailed information on mounting behavior and the dominance hierarchy. These extended materials were available, at least in one part of the exhibit, to educate people if they chose to read it. At both zoos though, these materials were only available on one side of the exhibit. Since visitors often do 89

not walk around the entire exhibit, this information would be more beneficial if it was Located

on all sides. Another problem with educating the public at the zoo is that often visitors do

not take the time to read the material provided. At some zoological parks, Busch Gardens, in

Tampa, Florida, for example, educational material is displayed via videos of the animals in their natural habitat. This is a stimulating way for the public to learn about the animals on exhibit. If these options are not possible for either zoo, perhaps a detailed guidebook, included in the ticket price, communicating specifics about each species and conservation efforts would be beneficial. At present it appears that to the majority of the public, zoos are mainly just entertainment facilities. The American Zoological Association, of which both zoos are members, states that their mission is education and conservation (Wiese and

Hutchens 1997). For the zoo to truly be considered an educational center, rather than an entertainment facility, it needs to educate the majority of people who attend, not the minority.

This study is not in any way trying to belittle the current education efforts of either zoo.

Both zoos are doing a good job of trying to engage the public and each holds presentations and special events on the animals. However, it seems as though there is some resistance on the part of the public to view the zoo as an educational rather than entertainment center.

Therefore, it may be necessary to extend efforts (if possible on limited funding) to try to change these perceptions.

In addition to education, conservation is the other main goal of zoos. Through the

Species Survival Plan, zoos manage the genetic viability of the captive population. This study has shown that the behavioral repertoire of captive Japanese macaques is very similar, at least in terms of the types of behaviors displayed, to that of wild monkeys. Preserving these species-specific behaviors should be the main goal of all captive programs (Fa 1986). 90

With a few alterations both zoos could encourage species-specific behaviors that are at least functionally more similar to the same time budget as wild conspecifics. The conservation of the natural behavior of captive primates is crucial in that almost all primates, including

Japanese macaques are being threatened by human activities. Though at the moment

Japanese macaques exist in the wild, their status is threatened. Their status was considered endangered in 1996 and they were placed on the Red List by the International Union for

Conservation of Nature and Natural Resources (IUCN). Japanese scientists, though, have challenged this classification, and thus CITES and IUCN currently list this species as having deficient data. However, even if this species is not considered in danger of extinction at the moment, they are threatened, and considering human population and agricultural pressures, there is no reason to assume their status will improve.

For many species of primates, their future as wild, free animals is in jeopardy. Human population growth and demands are pushing these animals out of their natural habitats.

Many of the great apes in particular, are expected to go extinct in the wild within the next 50 years unless drastic changes are implemented. Shumaker (2003) notes that wild orangutans may be extinct before the year 2020. It does not appear that humans are going to change our way of living fast enough to save many of these wild primates. Many of these primates will be extinct in the wild before people realize what they have lost.

Zoos offer hope to conservationists. If the natural behaviors and genetic viability of these animals are maintained, it is possible that some species can be reintroduced back into the wild. Though transplanting wild Japanese macaques back into the wild may not be an option at this point in time (nor desired by Japanese residents, since these monkeys are considered a pest by some); it is possible that sometime in the future this may be an option. 91

Reintroduction programs will not be successful if the animals have lost the ability to survive in the wild due to the loss of species-specific behaviors (Stoinski et al. 1997). If these primates along with many others eventually go extinct in the wild, captivity (or confined free-ranging situations) may be all that is left of these populations. Though it certainly can be strongly (and justifiably) argued that animals as intelligent as monkeys and apes should not be kept in captivity, it would be even more devastating to the world if they were lost from the wild if we did not have the captive populations. The captive populations of all endangered animals give conservationists the hope that even if one day these animals are extinguished from the wild, they will not be lost forever. Perhaps one day, if we are able to preserve their natural state, we can reintroduce them into the wild and repair what we have destroyed. 92

APPENDIX. ETHOGRAM

Behavior Description Includes: (both submission and dominance behavior) Attack physical chase/possible wounding Displacement — an individual is supplanted (forced t0 move) Display —shaking Of trees/branches in exaggerated fashion Agonism Dominance mounts —one monkey (mounter) stands against the rear of another (mountee), placing hands on the mountee's back and feet against the mountee's feet/legs Face threats -mouth open, teeth covered by lips Grimace —lips pulled back, teeth exposed Pelage and skin is cleaned and inspected by another monkey, using Allogroom fingers or mouth Autogroom Cleaning own pelage and skin, using fingers or mouth Feed Ingestion of food items or water Inactivity No movement -sitting, lying, or sleeping Moving by walking, running, climbing, jumping, swimming or Move wading more than two meters from original location The handling of an object with apparent lack of ingestion. Includes Obi ect . . biting, picking, and licking at cage, walls, trees, garbage, small Manipulate animals and toys Social affiliation with other individuals, involves cuffing (lightly Play striking with both hands) and jumping on each other, all with a play face (relaxed open mouth, teeth covered by lips) Includes either mating (series mount consisting of multiple mounts Sex ua1 over an extended period of time resulting in e' aculation or self- Activit y ~ ) manip ulation of genitals 93

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ACKNOWLEDGEMENTS

I would like to thank the Minnesota and Blank Park Zoos for allowing research to be conducted at their facilities. I also am grateful to the Japanese macaque keepers for patiently answering my questions.

I am especially indebted to Dr. Jill Pruetz. Her guidance has been invaluable on this project and throughout my studies at Iowa State. The advice of Dr. Matthew Hill and Dr.

Bonnie Bowen is also greatly appreciated.

This thesis could not have been finished without the support of my family. In particular, I dedicate this thesis to my husband, Dustin, who has always been a source of encouragement throughout my studies.